Download A review of factors affecting the population dynamics of jack pine

Popul Ecol (2000) 42:243–256
© The Society of Population Ecology and Springer-Verlag Tokyo 2000
SPECIAL FEATURE: REVIEW
Deborah G. McCullough
A review of factors affecting the population dynamics of jack pine budworm
(Choristoneura pinus pinus Freeman)
Received: October 1, 1999 / Accepted: September 22, 2000
Abstract Jack pine budworm (Choristoneura pinus pinus
Free.) (Lepidoptera: Tortricidae) is a native insect that
periodically defoliates areas of jack pine (Pinus banksiana
Lamb.) in the subboreal forests of North America east of
the Rocky Mountains. Outbreaks of jack pine budworm
generally occur at 6- to 12-year intervals and collapse after
2–4 years. Periodicity of outbreaks varies and is associated
with site-related factors. Survival of early-instar larvae during spring dispersal is tied to the abundance of pollen cones
(microsporangiate strobili), which provide a refuge for larvae until current-year needles expand. Jack pine trees that
have been heavily defoliated produce few pollen cones in
the following year, often resulting in high mortality of earlystage larvae. A diverse guild of generalist parasitoids attack
jack pine budworm, but only a few species account for most
mortality in any area. Collapsing jack pine budworm populations are characterized by sharp declines in early instar
survival, coupled with an increased rate of parasitism in the
late larval and pupal stages. The reciprocal interaction between heavy defoliation and low pollen cone production,
and increased parasitism of late-stage larvae or pupae, are
consistent with second-order density dependence factors
identified in analysis of a long-term population data set.
Since the 1950s, several jack pine budworm outbreaks have
been roughly synchronous over a large geographic area,
suggesting that Moran effect processes, as well as moth
dispersal or other factors, may be involved in jack pine
budworm dynamics. Although the short duration of outbreaks enables most trees to recover, over time dead trees
and top-killed trees accumulate in jack pine stands. Jack
pine is well adapted to fire and when fires ignite, the accumulation of dead trees and woody debris often leads to
intense wildfires followed by prolific regeneration. The
D.G. McCullough
Department of Entomology and Department of Forestry, 243
Natural Science Building, Michigan State University, East Lansing,
MI 48824-1115, USA
Tel. 11-517-355-7445; Fax 11-517-353-4354
e-mail: [email protected]
three-way interaction of jack pine, jack pine budworm, and
fire ultimately serves to maintain vigorous stands and
ensures continued hosts for jack pine budworm.
Key words Jack pine · Pollen cones · Parasitoids · Moran
effect · Fire
Introduction
Jack pine (Pinus banksiana Lamb.) is a common tree
throughout the subboreal forests of North America east of
the Rocky Mountains. It occupies close to 1 million ha in
the Great Lakes states of Michigan, Wisconsin, and Minnesota, and is the most widely distributed pine in Canada,
ranging from the Atlantic coast west into Alberta (Rudolph
and Laidly 1990). Jack pine grows rapidly as a young tree
but is relatively short lived (Harcomb 1987). It has a notably
high nutrient-use efficiency, and merchantable stands can
be produced on relatively poor sites that most other species
do not tolerate (Alban et al. 1978; Cayford 1970; Foster and
Morrison 1976). In the Great Lakes region, jack pine is
most commonly found on sites with sandy soils and relatively low moisture and nutrient availability but occupies a
greater range of sites in Canada. Economically, jack pine is
an important source of pulpwood in the United States and is
harvested for sawtimber and pulp in Canada.
Jack pine budworm (Choristoneura pinus pinus Freeman) (Lepidoptera: Tortricidae), a native, univoltine defoliator, is arguably the most important insect pest of jack
pine and may exert substantial influence on stand structure
(Volney 1998). Jack pine is the primary host of jack pine
budworm (JPBW), but larvae will also consume red pine
(Pinus resinosa Ait.), eastern white pine (Pinus strobus L.),
and Scotch pine (Pinus sylvestris L.), usually when those
species are adjacent to or mixed with jack pine (Kulman
and Hodson 1961a).
Jack pine budworm is similar in appearance and life
cycle to other conifer-feeding budworms, including spruce
budworm (Choristoneura fumiferana Clem.), western
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Table 1. Time periods when jack pine budworm outbreaks were recorded in the Great Lakes states (encompassing the lower and upper
peninsulas of Michigan, Minnesota, and two regions of Wisconsin), and the Canadian provinces of Manitoba and Saskatchewan
Period
Lower
Michigana
Upper
Michigana
Minnesotaa
Northwest
Wisconsina
Northeast
Wisconsina
Manitobab
Early to mid-1950s
Early 1960s
Mid- to late 1960s
Early to mid-1970s
Late 1970s
Early to mid-1980s
Early 1990s
X
X
X
X
X
X
X
–d
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
–d
X
X
–d
Central
Saskatchewanc
Records represent the occurrence of heavy defoliation in at least one area of each region, rather than actual population estimates
a
Occurrence of outbreaks in Michigan, Minnesota and Wisconsin based on reports published by the Michigan Dept. of Conservation (later
renamed Michigan Dept. of Natural Resources), the Minnesota Dept. of Natural Resources, and the Wisconsin Dept. of Natural Resources
b
Outbreaks in Manitoba since 1950 reported by Volney (1988) based on defoliation maps and reports from the Forest Insect and Disease Survey
(Canadian Forest Service) and provincial forest pest reports
c
Outbreaks in central Saskatchewan since 1950 reported by Volney (1998) based on defoliation maps and reports from the Forest Insect and
Disease Survey (Canadian Forest Service) and tree ring analysis
d
Data not available
spruce budworm (C. occidentalis Freeman), and C. pinus
maritana, a subspecies associated with localized areas of
Pinus virginiana Mill. in northeastern states (Freeman
1967). It was first recognized as a distinct form by Graham
(1935) on the basis of biological and behavioral traits. Taxonomic distinctions specific to JPBW were later published by
Freeman (1953), but later work showed that morphological
features did not always permit species identification
(Harvey 1985). Surveys of genetic variation using amplified
mitochondrial DNA and analysis of allozyme frequency
indicated that C. pinus pinus is a distinct species that is more
closely related to western species such as C. occidentalis
than to C. fumiferana (Harvey 1996; Sperling and Hickey
1995).
Outbreaks of JPBW typically occur at 6- to 12-year intervals (Howse and Meating 1995; Ives 1981; Moody 1986;
Volney 1988; Volney and McCullough 1994). Some outbreaks are relatively localized while others are extensive,
affecting much of the jack pine range (Table 1). At a regional level, JPBW populations may be high for 5–6 years
or occasionally longer. Within a region, however, outbreak
populations persist in specific localities for only 2–4 years,
and severe defoliation rarely occurs for more than 1 year
in any stand (Gross and Meating 1994; McCullough et al.
1996; Weber 1995). This pattern enables most jack pine
trees, which carry only 2–3 years of foliage, to recover to
preoutbreak growth rates 2 years after defoliation ceases
(Kulman et al. 1963; Conway et al. 1999b). However, tree
mortality following outbreaks can be substantial. Impact
studies found that, on average, roughly 15% of trees died
following recent outbreaks in Canada and Michigan
(Conway et al. 1999a; Gross and Meating 1994). Heavy
defoliation in the upper crown can also lead to dead terminal leaders and tops. An average of 15%–20% of surviving
trees can be topkilled during a single outbreak (Conway
et al. 1999a; Gross 1992), and topkilled trees may be most
likely to succumb during subsequent outbreaks (Conway
et al. 1999b).
Changes in the abundance of JPBW over time and space,
the rate of change, and the processes that drive those
changes are of interest to ecologists, forest entomologists,
and resource managers. A complex of factors including pollen cone production and other aspects of host plant quality,
natural enemies, and weather undoubtedly interact to affect
JPBW population dynamics at spatial scales ranging from
the level of individual trees to forest stands to entire landscapes. Our understanding of these factors is increasing as
data are acquired from empirical studies largely driven by
the economic consequences of JPBW outbreaks. Many
interesting questions remain, however, and answers are
needed to identify the mechanisms underlying JPBW population behavior, accurately predict outbreaks, and estimate
how silvicultural or natural disturbances may affect JPBW
dynamics. This paper briefly reviews JPBW biology and
previous efforts to evaluate JPBW population dynamics
and examines factors that contribute to stage-specific mortality. The objectives are to present an overview of what has
been learned about JPBW population dynamics, identify
knowledge gaps, and assess the role of JPBW in the jack
pine ecosystem.
Jack pine budworm life cycle
Jack pine budworm biology has been described by several
authors (Graham 1935; LeJuene 1950; LeJeune and Black
1950; Kulman and Hodson 1961b). Eggs are laid in masses
consisting of overlapping rows of eggs on needles in midsummer. Egg masses are usually found on older needles,
perhaps because these needles are more widely spread or
stiffer than current-year needles (Graham 1935). Mean
number of eggs per mass ranged from 38 to 59 in field
collections (Fowler and Simmons 1987) and from 32 to 41
when budworms were reared in the laboratory (Campbell
1953). Eggs hatch in 1–2 weeks.
On hatching, neonate larvae seek sheltered locations
under bark scales or in crevices on branches and the stem.
Larvae spin silk hibernaculae, molt, then enter an obligate
diapause and overwinter as second instars without feeding
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(Nealis 1987). Termination of diapause and emergence of
larvae from hibernaculae the following spring is influenced
by the duration of the cold period (Nealis 1995) and proceeds faster at higher spring temperatures (Lysyk 1989).
After leaving the hibernaculae in spring, the positively
phototrophic larvae move toward the peripheral shoots of
the branch or leader. If the larvae encounter pollen cones
(microsporangiate strobili), they will move into the cones
and begin feeding on the pollen, a trait explored in more
detail later. When budworm populations are dense, many
larvae may inhabit a single pollen cone for several days. If
pollen cones are not encountered and current-year foliage is
not yet available, larvae usually disperse by dropping from
peripheral shoots on a single strand of silk. Larvae that blow
onto adjacent or nearby trees or land on understory trees
will resume the search for suitable feeding sites, whereas
early instars that land on the ground are probably doomed.
Mortality of dispersing larvae may be high, especially in
stands where pollen cones are scarce (Nealis and Lomic
1994) or where trees are widely spaced (Batzer and
Jennings 1980). As current-year shoots expand and pollen is
shed, most larvae move out and feed on the growing needles
for roughly 6 weeks, passing through a total of seven instars
(LeJeune 1950; Nealis 1987).
Larvae feed preferentially on current-year foliage, consuming 1- and 2-year-old needles only after most currentyear foliage has been consumed. Shoots are frequently
webbed together with silk, creating feeding shelters. The
final two instars consume the most foliage (Kulman and
Hodson 1962), and their density is consistently associated
with defoliation levels (Nealis et al. 1997; Scarr 1995).
Larvae are wasteful feeders, usually feeding on all but the
midrib of the basal portion of needles, then clipping off the
needle, leaving the distal end untouched. When foliar nitrogen levels are low, larvae compensate by consuming an
increased amount of foliage (McCullough and Kulman
1991a,b). Pupation occurs on the trees in July, and adults
emerge within 1–2 weeks.
Adults live only a few days and are nonfeeding, although
they may imbibe water or nectar as does the spruce budworm (Miller 1987). A female-produced sex pheromone
(Sanders 1971) attracts males and may serve as a barrier to
hybridization of spruce and jack pine budworms (Silk and
Kuenen 1988). Nonhost volatiles may deter oviposition on
unsuitable hosts, but ovipositional host specificity for JPBW
appears to be more dependent on physical cues such as
needle length than chemical cues (Grant and Langevin
1994). Estimates of lifetime fecundity from field or labreared pupae indicate that female moths may lay up to
130–150 eggs (Foltz et al. 1972; Grant and Langevin 1994;
Johnson 1968; Nealis 1995).
Both sexes are capable of flight, but little is known about
the frequency or extent of moth dispersal and how dispersal
may be influenced by stand- or landscape-level factors. Jack
pine budworm moths closely resemble C. occidentalis and
C. fumiferana moths, which are known to be capable of
long-range dispersal or dissemination by wind (Campbell
1993; Greenbank 1957; Greenbank et al. 1980). Intriguing
notes related to moth flight occasionally appear in annual
forest pest reports produced by state forest management
agencies. For example, in 1994, a “heavy flight” of moths
was observed in Wisconsin (Wisconsin Dept. of Natural
Resources 1994), and a 1965 report noted that JPBW moths
were so numerous on the evenings of July 22 and July 23
that some motels and restaurants in northern lower Michigan had to close (Michigan Dept. of Conservation 1965). In
a life table study during a Minnesota outbreak, estimates of
realized fecundity (defined as the number of eggs in cohort
2 for each female in cohort 1) varied substantially, from 17
to 357 eggs per female (Foltz et al. 1972). This variation may
represent not only differential vigor and longevity of female
moths, but also stand or landscape factors that affect
dispersal or interception of flying moths (Volney 1989).
Intensive population surveys during a JPBW outbreak
in Wisconsin indicated that egg mass density was lower in
heavily defoliated stands than in nearby stands with light
defoliation (Weber 1995), although within a stand, egg density can be similar on heavily and lightly defoliated trees
(Scarr 1995). Weber (1995) speculated that female moths
laid a portion of their eggs in the stand where they developed, then emigrated to less-defoliated stands to lay additional eggs. Spruce budworm moths can exhibit similar
behavior; gravid moths laid roughly 50% of their eggs
before their first flight (Sanders and Lucuik 1975). When
potential effects of landscape-level factors on JPBW defoliation were evaluated in Michigan, Kouki et al. (1997) determined that stands sustained heavier JPBW defoliation
than expected if they were adjacent to very young trees, an
opening, or a road. This edge effect could result if dispersing moths were intercepted by edge trees and subsequently
oviposited within the stand.
Studies of JPBW population dynamics
Although few long-term data sets are available, the economic importance of JPBW defoliation and apparent periodicity of outbreaks have encouraged scientists to examine
mortality factors and variables driving JPBW dynamics.
Past studies include short-term investigations that used a
life table approach to identify stage-specific mortality, and
analysis of long-term population data from Wisconsin and
aerially mapped defoliation data from Canada.
Two related studies conducted in 1965–1968 during a
JPBW outbreak in the Lake States region used counts of
eggs, larval stages, and pupae to develop life tables for 29
JPBW cohorts in Michigan (Foltz et al. 1972) and 32 cohorts
in Minnesota (Batzer and Jennings 1980). Both studies used
regression and components of variance analysis to identify
the stages most closely associated with the overall population trend. Results from these studies are useful, although
methodological problems such as pooling data from numerous sites and the short time series represented by the data
limited the ability of the authors to explore causal factors
(Nealis 1995).
In Michigan, Foltz et al. (1972) found that two variables,
survival of small larvae (the stage between egg counts and
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counts of small larvae the following spring) and survival of
large larvae (from large larval counts to the pupal stage),
varied substantially between increasing and decreasing
populations. Realized fecundity (defined as the number of
eggs in cohort 2 for each female in cohort 1) also entered
regressions. Together these variables accounted for 58%–
93% of the variation in population trend. Covariance
analysis showed that survival of small larvae and realized
fecundity were negatively associated with population trend,
suggesting that density-dependent factors may have operated on these stages. They also found a positive covariance
between survival of large larvae and population trend, perhaps indicative of inverse density dependence in peaking
populations.
Batzer and Jennings (1980) used somewhat different
sampling and analytical methods in their Minnesota study.
They found that survival during large larval, pupal, and
small larval stages were most strongly related to overall
generational survival. However, the importance of stagespecific mortality depended on the density of the population. At low population densities, survival of early stages
was most important, whereas at high densities large larval
and pupal survival were most important. Unlike Foltz et al.
(1972), the methods used by Batzer and Jennings (1980)
enabled them to distinguish among mortality factors acting
on eggs and on young larvae in the fall and spring. They
found that mortality of small larvae dispersing in spring
was much more important than mortality of eggs or newly
hatched larvae. In addition, mortality of larvae during
spring dispersal was strongly and inversely related to tree
density.
Volney (1988) examined periodicity of JPBW defoliation for a 50-year period using defoliation maps and reports
primarily collected by the Canadian Forest Service, Forest
Insect and Disease Survey (FIDS) in Manitoba and
Saskatchewan. He recognized potential limitations in the
data because populations were not measured directly and
extensive defoliation was more likely to be reported than
localized outbreaks. Even so, six distinct periods of outbreaks could be identified through 1986, but the last three
cycles, dating from the 1960s, appeared to be more extensive and severe than the earlier three cycles. An outbreak
periodicity of 10 years was statistically significant but was
confounded with fire history in the region, and explained
less than 30% of the variability in the time-series plot of
defoliation severity. Autocorrelation functions (ACF) and
partial autocorrelation functions (PACF) were tested for
lags ranging from 1 to 25 years but explained little variation
in the time series data.
Volney and McCullough (1994) analyzed JPBW population data collected in 100–140 stands in northwestern Wisconsin over a 17- to 31-year time span. Counts of early stage
larvae (in pollen cones) provided the longest time series and
were pooled by township (93.2-km2 area) for analysis. The
time-series data were tested for evidence of significant
periodicity, feedbacks, and density-dependent population
regulation using Fourier analysis, calculation of ACF and
PACF, and Turchin’s (1990) modification of Ricker’s
model. In addition, they evaluated the association between
population periodicity and habitat type, using a detailed
system based on gradients of moisture and nutrient availability in Wisconsin forests (Kotar et al. 1988).
Results indicated that both delayed and densitydependent processes were operating in the JPBW populations. In 20 of 31 townships, JPBW outbreak cycles
significantly oscillated at 5-, 6-, or 10-year intervals. Secondorder coefficients were negative in 28 of 31 townships and
accounted for more variation than first-order coefficients,
indicating that second-order (lagged) density dependence
contributed most strongly to the dynamics. There was a
strong association between JPBW population behavior and
habitat type. Outbreak frequency was consistently related
to soil moisture, with 5- to 6-year cycles occurring on the
driest sites, 10-year cycles occurring on intermediate sites,
and a general lack of periodicity on relatively mesic sites.
Evidence for density-dependent regulation was strongest in
xeric areas with chronically high JPBW densities and frequent outbreaks and weaker in areas near the periphery of
the jack pine range in northwestern Wisconsin.
Ecological factors affecting jack pine budworm
Several studies have evaluated interactions between JPBW
and jack pine and how factors such as natural enemies or
weather may influence populations. Much of this research
was completed during outbreaks, and information on
interactions and factors regulating populations between
outbreaks is scarce. Interesting relationships have been
identified, however, and suggest that pollen cone abundance and late-stage parasitism may be particularly influential in affecting JPBW dynamics at local scales while Moran
effect processes (Royama 1992; see following “Outbreak
Synchronicity” section) may account for the apparent synchrony of some outbreaks across regions.
Host suitability: pollen cones
A unique association between JPBW outbreaks and pollen
cone production was recognized early (Graham 1935;
LeJeune 1950) and has continued to intrigue forest entomologists. Recent evidence indicates that pollen cones play
a prominent role in JPBW dynamics by providing a critical
resource for JPBW larvae following emergence from
hibernaculae in early spring (Batzer and Jennings 1980;
Nealis and Lomic 1994). Emergence of overwintered larvae
is initiated in response to increasing air temperature,
whereas bud break and foliage expansion are strongly
influenced by soil temperature as well as air temperature
(Volney 1989). Unlike spruce budworm larvae, JPBW larvae do not readily mine buds or 1-year-old needles. Therefore, in years when larval activity precedes expansion of
current-year needles, pollen cones provide food, an apparently favorable microhabitat, and perhaps some protection
from potential natural enemies (Batzer and Jennings 1980;
Nealis and Lomic 1994; Nealis et al. 1997), although the
247
latter has not been specifically addressed. As a food source,
pollen is high in nitrogen and lacks secondary compounds,
lignin, cuticular waxes, or other defenses. Pollen is usually
shed by the time larvae are in the third instar, and most
larvae remain in the cones only until current-year foliage
begins to expand. Some larvae remain in silk webs in pollen
cones through later stages, venturing out occasionally to
feed on foliage (LeJeune 1950).
Trees that have been severely defoliated, however, produce few if any pollen cones the following year (Foltz et al.
1972; Graham 1935; Hodson and Zehngraff 1946; Kulman
et al. 1963; Nealis and Lomic 1994; Nealis et al. 1997). This
decrease results in increased spring dispersal and low survival of early-instar larvae in previously defoliated stands
with few pollen cones compared to undefoliated stands with
a greater abundance of pollen cones. Data collected during
recent JPBW outbreaks in Ontario and Michigan showed
that survival between overwintering and early-instar stages
was a direct function of pollen cone abundance in the stand
(Nealis and Lomic 1994; Nealis et al. 1997). Thus, the rise
and fall in early-instar abundance over the course of an
outbreak could reflect the influence of pollen cones on
JPBW larvae and the reciprocal, negative influence of larvae on pollen cone production. Such a relationship could
partially account for the second-order (lagged) densitydependent factor detected by Volney and McCullough
(1994) in their analysis of long-term population data from
Wisconsin (Nealis 1995).
The association between pollen cones and budworm survival can sometimes vary over the course of an outbreak,
however. In the Minnesota life table study, for example,
Batzer and Jennings (1980) found, in the first year of the
outbreak, that survival of small larvae was directly related
to abundance of pollen cones. In the second year, small
and large larvae were abundant despite a scarcity of pollen
cones. In the third year, previously defoliated trees had
recovered and pollen cones were nearly as abundant as in
year 1. Despite relatively high survival of small larvae in the
stands with abundant pollen cones, the JPBW population
crashed because of unknown factors that caused high
mortality of late-instar larvae. This pattern led Batzer and
Jennings (1980) to conclude that survival during early stages
had relatively little influence on overall generation survival
when population densities were high.
Surprisingly, despite the strong association between pollen cones and early larval survival during outbreaks and the
high nitrogen content of pollen, pollen cones do not appear
to directly enhance larval development or fecundity. In
laboratory tests, larvae feeding in pollen cones developed
more slowly than larvae reared on foliage (Hansen 1988;
Johnson 1968; LeJeune 1950). Late-stage larvae collected
from trees with abundant pollen cones produced an average
of 79 eggs per female, while larvae collected from trees
without pollen cones produced 150 eggs per female on average (Johnson 1968). In their Minnesota study, Batzer and
Jennings (1980) recorded higher fecundity in the second
year of the outbreak, when pollen cones were scarce, than
in the first year when pollen cones were abundant. Nevertheless, in laboratory tests, JPBW larvae that were given a
choice of shoots consistently preferred to feed in pollen
cones rather than on vegetative shoots, even after new
needles became available (Lomic and Nealis 1996; Nealis
and Lomic 1994). Survival of the larvae reared on vegetative shoots was initially poorer than survival on shoots with
pollen cones, but once buds broke and new needles were
available, survival rates were equal. Volney (1988) hypothesized that relatively slow growth of larvae in pollen cones
may provide a mechanism to ensure that adult stages are
synchronized for mating, while maintaining variability in
emergence from hibernaculae to ensure that some portion
of the population will have food available.
Although there is no doubt that jack pine trees produce
few, if any, pollen cones the year after heavy defoliation,
pollen cone formation in other years can be affected by
numerous factors. Abundance of pollen cones on individual
trees and at the stand level varies considerably from year
to year (Hodson and Zehngraff 1946; McCullough and
Kulman 1991b; Nealis et al. 1997; Scarr 1995). This variation
has been attributed to numerous site and stand characteristics, including tree age and availability of light, water, and
nutrients (Batzer and Jennings 1980; Graham 1935; Hodson
and Zehngraff 1946; Kouki et al. 1997; Volney 1988; Weber
1995). Guidelines for jack pine managers often stress removal of full-canopied orchard trees, as well as suppressed,
low-vigor trees, to limit availability of pollen cones (Jones
and Campbell 1986; McCullough et al. 1994; Weber 1986,
1995). Volney (1988) speculated that the greater severity
of JPBW defoliation in Manitoba and Saskatchewan in
the past 30 years might reflect efforts to control forest
fires, subsequently leading to more pollen cone production
in aging jack pine stands, and hence higher budworm
densities. However, although mature trees generally produce more pollen cones than sapling or pole-sized trees,
sizable pollen cone crops have also been observed on trees
less than 10 years old (Hodson and Zehngraff 1946;
McCullough and Kulman 1991b; Rudolph and Laidly 1990).
Nitrogen fertilizer applied to young trees on a site with low
nitrogen availability stimulated pollen cone production but
had little effect on other sites with higher nitrogen levels
(McCullough and Kulman 1991b). Mechanistic processes
that determine pollen cone production have not been described for jack pine, although research with other coniferous species suggests that giberellins promote differentiation
of buds into pollen cone buds (Harrison and Owens 1992).
Given the important role that pollen cones appear to play in
JPBW dynamics, a better understanding of pollen cone formation and how this process is affected by tree age or site
and stand variables would be useful.
Host suitability: foliage quality
Other aspects of host suitability such as foliage quality may
also influence survival or fecundity of JPBW and ultimately
affect dynamics of JPBW populations. Scarr (1995) observed that green, undefoliated trees were consistently
present in stands that were otherwise extensively defoliated
during a 1980s JPBW outbreak in Ontario and Michigan.
248
He related density of eggs and larval stages on undefoliated
and defoliated trees to variables such as tree vigor, phenology of bud break and shoot expansion, and pollen cone
abundance. Although numbers of eggs and small larvae
were similar on defoliated and undefoliated trees, pupal
densities were much lower on undefoliated trees, indicating
that late-stage larval mortality or emigration was greater on
some trees than others. There were no consistent differences in pollen cone production or bud break phenology,
leaving Scarr (1995) to speculate that foliage quality or
subtle microsite factors might account for the apparent resistance of some trees.
Because nitrogen is a critical nutrient for most phytophagous insects including other Choristoneura species (Cates et
al. 1987; Mattson 1980) and is typically limited on the sandy
soils where jack pine often occurs (Rudolf 1958; Wilde et al.
1964), McCullough and Kulman (1991a) hypothesized that
foliar nitrogen levels might affect JPBW survival or fecundity. Current-year foliage was collected from 80 young trees
in four stands in northwestern Wisconsin during the summer while larvae were feeding, and again in autumn when
trees were dormant. Foliar nitrogen levels of trees in stands
that had regenerated after clear-cutting were consistently
12% higher than those of trees in stands that regenerated
after wildfire. Survival of caged JPBW larvae was also significantly higher on clear-cut area trees than burned area
trees, despite increased foliage consumption by larvae on
the low-nitrogen trees. Foliar monoterpenes were 25%
higher on clear-cut area trees than burned area trees and
were significantly correlated with nitrogen levels in this
and related studies (McCullough and Kulman 1991b;
McCullough et al. 1993). However, monoterpenes did not
appear to negatively affect survival, development, or pupal
weight of the budworms.
Wallin and Raffa (1998) sampled foliage in August to
quantify monoterpenes and nutrients in 12 young jack
pine trees in central Wisconsin that had been defoliated
by JPBW. Total monoterpenes were approximately 10%
higher in the distal portions of needles. Three compounds,
limonene, carene, and myrcene, were greater in the distal
needle portion while levels of alpha-pinene and beta-pinene
were similar or greater in the basal portion. The authors
speculated that by feeding primarily on the basal portions
of needles, JPBW larvae may avoid ingesting high levels of
some monoterpenes. However, it is not clear whether levels
and distribution of monoterpenes in August are the same as
they would be in June or early July, when most JPBW are
feeding. Monoterpene synthesis and accumulation can
vary depending on phenological development of foliage,
nitrogen availability, or other factors (Bernard-Dagan 1988;
Gershenzon 1984; McCullough and Kulman 1991b; Muzika
et al. 1989).
Several studies have suggested that availability of water
to host trees or foliage moisture may influence interactions
between jack pine and JPBW. When larvae were caged on
young jack pine trees in Wisconsin, tree water potential and
foliage moisture were negatively related to larval survival
but positively related to pupal weight in regression models
(McCullough and Kulman 1991a). Clancy et al. (1980)
noted that susceptibility of Wisconsin stands to JPBW defoliation appeared to be related to soil type and presumably
water availability, but they did not explore this association
further. In their analysis of long-term population data from
the same Wisconsin stands, Volney and McCullough (1994)
found that population behavior was associated with differences in water availability along a gradient of habitat types.
It is not clear, however, whether water availability directly
affects foliage quality for budworm larvae or if it appears to
be important because of indirect associations with other
host characteristics.
Natural enemies
Parasitoids
Parasitoids appear to be the most important group of natural enemies affecting JPBW and may play a prominent role
in the dynamics of an outbreak cycle. At least ten different
studies involving JPBW parasitoids have been conducted,
and most occurred during either the peak or collapse of an
outbreak (Allen et al. 1969; Benjamin and Drooz 1954;
Brandt and Melvin 1970; Dixon and Benjamin 1963; Drooz
and Benjamin 1956; Elliott et al. 1986; Foltz et al. 1972;
Kulman and Hodson 1961c; Nealis 1991, 1995). Results
show that the JPBW parasitoid guild is characterized by a
high degree of species diversity, including 32 hymenopterous parasitoids, 16 dipterous species, and 14 known or suspected hyperparasitoids (Nealis 1995). Composition of the
parasitoid guild varied among the studies, but only a few
species accounted for most of the parasitism in any of the
populations (Allen et al. 1969; Dixon and Benjamin 1963;
Nealis 1991). Rates of parasitism by specific species often
varied between basal and distal sections of branches, among
canopy levels, between suppressed and dominant trees, and
between trees along the edge of a stand versus the interior
of the stand (Allen et al. 1969; Kulman and Hodson 1961c;
Nealis and Lysyk 1988).
Early stages of JPBW are attacked by several parasitoids, but this mortality generally did not impact overall
population fluctuations. A single egg parasitoid,
Trichogramma minutum Riley, was often recovered, but
had little effect on JPBW populations except at one Wisconsin site, where 62% of the eggs were parasitized in 1 year
(Dixon and Benjamin 1963). Two larval parasitoids, the
ichneumonid Glypta fumiferanae (Vier.) and the braconid
Apanteles fumiferanae Vier., were ubiquitous and generally
abundant in all surveys. These species oviposit in first or
second instars, overwinter in the host, then emerge from
mostly fourth and fifth instars (Allen et al. 1969; Dixon and
Benjamin 1963; Nealis 1991). Although the two species
parasitized a relatively high proportion of JPBW larvae
compared to other species, parasitism rates were similar in
peaking and collapsing populations, indicating that they had
little effect on JPBW population trends (Allen et al. 1969;
Nealis 1991, 1995).
In contrast, parasitoids of late-instar larvae and pupae
may play a key role in JPBW dynamics by speeding the
249
collapse of JPBW populations (Allen et al. 1969). An increase in the apparent rate of late-instar or pupal parasitism
as JPBW populations declined or collapsed was documented in Michigan and Wisconsin populations (Allen et
al. 1969; Benjamin and Drooz 1954; Dixon and Benjamin
1963), although the parasitoids responsible for the mortality
differed among the populations. In Ontario, Nealis (1991)
similarly observed that high rates of late-instar mortality
attributed to the braconid Meteorous trachynotus Vier. and
the tachinid Lypha setifacies (West.) occurred only in collapsing JPBW populations but not during the peak year of
the outbreak.
Many of the larval and pupal parasitoids that attack
JPBW are generalists, indicating that their abundance may
be affected by the availability of alternative hosts. Spruce
budworm is undoubtedly one of the alternate hosts; typically, the most abundant species recovered from JPBW are
also common parasitoids of spruce budworm (Benjamin
and Drooz 1954; Nealis 1991). However, the phenological
development of spruce budworm is similar to that of JPBW,
suggesting that spruce budworm could effectively function
as a competing sink for shared parasitoid species. The identity of other alternate hosts has not been well addressed
despite recognition that several of the late-instar or pupal
parasitoids, including L. setifacies, have two or more generations per year (Allen et al. 1969).
Influence of parasitoids on JPBW dynamics
Evidence suggests that the combined effects of late-instar or
pupal parasitism and pollen cone availability may explain
much of the dynamics of JPBW populations once an outbreak arises in a localized area (Allen et al. 1969; Nealis
1995). Second-order, density-dependent mortality processes that were detected in the long-term JPBW population data from Wisconsin (Volney and McCullough 1994)
could reflect the dependence of early-instar JPBW larvae
on pollen cones and the reduced production of pollen cones
the year after heavy defoliation (Kulman et al. 1963; Nealis
and Lomic 1994). In addition, rapid declines in early-instar
abundance combined with increased rates of late-instar
larval and pupal parasitism would account for the typical
collapse of JPBW outbreaks after 2 to 3 years (Allen et al.
1969; Nealis 1995).
Nealis and Lomic (1994) hypothesized that these patterns may also account for differences between oscillations
of JPBW and spruce budworm populations. Jack pine budworm populations are characterized by relatively frequent
outbreaks at 6- to 12-year intervals, and periodicity varies
with local site or stand conditions (Volney and McCullough
1994). Although spruce budworm populations share much
of the same parasitoid guild, populations typically oscillate
at intervals of 35 years, often across a larger geographic
area. Nealis and Lomic (1994) speculated that densitydependent processes do not operate strongly on earlyinstar spruce budworm larvae because they can mine buds
and older needles and do not rely on pollen cones. A longer
period of time is required, therefore, before apparent rates
of parasitism increase and, in combination with other
factors, bring about the collapse of a spruce budworm
outbreak.
Predators
Only a few studies have addressed predation of JPBW
by either vertebrate or invertebrate predators. Innes et
al. (1990) suggested that abundance of an insectivorous
shrew may have increased in response to a JPBW outbreak
in Ontario, but they did not directly observe shrews feeding
on JPBW. Feeding behavior and the overall impact of bird
predation were monitored in northern Michigan in 1965–
1967 (Mattson et al. 1968; Simmons and Sloan 1974; Sloan
and Simmons 1973). The chipping sparrow (Spizella
passerina [Bechstein]) was the most abundant bird in a
jack pine stand with a low JPBW population and another
stand experiencing an outbreak (Mattson et al. 1968). In
observation cages, chipping sparrows readily fed on exposed larvae and pupae and also captured larvae spinning
down on silk or enclosed in feeding shelters. Surprisingly,
the birds would not consume parasitized larvae or pupae,
which they distinguished by the immobility of parasitized
larvae and the rigidity of parasitized pupae (Sloan and
Simmons 1973). In the field studies (Mattson et al. 1968;
Simmons and Sloan 1974), most birds preyed on fifth-instar
or older JPBW larvae. Predation rates were affected by
JPBW density, past experience of the birds, and the exposure of the JPBW larvae. In a stand with an endemic
JPBW population, functional responses by residents and
immigration by nonresidents from surrounding plant communities resulted in predation rates of up to 65% of lateinstar larvae and pupae (Mattson et al. 1968). In larger
stands experiencing a JPBW outbreak, however, there was
little influx of nonresident birds and the impact of bird
predation was minimal (Mattson et al. 1968; Simmons and
Sloan 1974).
Ants and other invertebrates will prey on JPBW larvae
and pupae, but their impact is difficult to gauge, especially
in intervals between outbreaks. Graham (1935) noticed
that ants preyed on JPBW pupae that were placed on the
ground, but this mortality may be important only if high
numbers of pupae are dislodged from trees. In Wisconsin,
Jennings (1971) identified 6 species of ants that preyed on
JPBW larvae on the ground or when they attempted to
climb back up the tree stem after the larvae were intentionally dislodged from trees. Allen et al. (1970) observed
8 species of insects feeding on JPBW in field studies in
Michigan. A predatory pentatomid (Podisus serieventris
Uhler) was abundant and exhibited a numerical response to
JPBW larval density, although the authors concluded it
would be of limited importance during JPBW outbreaks. A
carpenter ant (Camponotus noveboracensis Fitch) and a
coccinellid (Anatis ocellata [L.]) were also encountered frequently. Allen et al. identified 51 species of spiders in the
jack pine stands but noted that spiders were not common in
dense stands or shaded conditions, and that heavy defoliation adversely affected the suitability of trees as habitat for
most spiders. Only 5 of the spider species were observed
preying on JPBW in the field.
250
Pathogens
Pathogens of JPBW have received scant attention and their
impact on population dynamics is not known. Allen et al.
(1969) specifically noted the absence of diseased larvae or
pupae in their rearing studies and field experiments. Batzer
and Jennings (1980) suggested that pathogens might account for some of the unknown late-instar mortality they
recorded in their life table study in Minnesota, but they did
not observe any cadavers with obvious signs of infection.
Jack pine budworm is susceptible to a nuclear polyhedrosis
virus isolated from spruce budworm (Stairs 1960) and two
microsporidia, Nosema fumiferana and a closely related
Nosema sp. isolated from JPBW larvae (Thomson 1959).
When the two microsporidia were incorporated into artificial diet, both reduced JPBW larval survival and pupal
weight and prolonged development (Wilson 1986). Volney
(1989) suggested that sublethal levels of pathogens such as
microsporidia might influence fecundity, which may be consistent with the unexplained reduction in egg mass size over
the course of the Minnesota outbreak observed by Batzer
and Jennings (1980).
Outbreak synchronicity
Evidence compiled from annual forest pest surveys conducted by forest management agencies suggests that the
occurrence of several JPBW outbreaks since 1950 has been
roughly synchronous in the Great Lakes states and the
Canadian province of Ontario (Table 1; Fig. 1). Historically,
JPBW populations were rarely monitored with the exception of northwestern Wisconsin, but heavy defoliation was
usually mapped or recorded and is presumably indicative
of high-density populations (Williams and Leibhold 1995).
The frequency and intensity of data collection varied,
depending on the budget and priorities of the responsible
agencies. Most records, especially from the Great Lakes
states, generally provided only a coarse estimate of defoliation, and detailed maps were rarely presented. Although
an outbreak might persist for 4 years or occasionally longer
within a state or province, heavy defoliation varied annually
among counties during the outbreak, and individual
stands rarely sustained more than a single year of heavy
defoliation.
Despite some limitations in the quality of the data, the
apparent synchrony of five major JPBW outbreaks in the
Great Lakes states and the Canadian province of Ontario
during the past 35–40 years is notable. Heavy JPBW defoliation was recorded in all three states plus Ontario in the
early to mid-1950s, early 1960s, late 1960s, mid- to late
1980s, and early 1990s (see Table 1, Fig. 1).
Defoliation records summarized by Volney (1988, 1998)
suggest outbreaks in the prairie provinces of Saskatchewan
and Manitoba have been somewhat less frequent (Table 1).
In Manitoba, four major outbreaks were recorded and three
of those periods – those occurring in the mid-1950s, the mid1960s, and the mid-1980s – overlap temporally with those
recorded in Ontario and the Lake States. Further to the
west in Saskatchewan, outbreaks occurred in the 1960s,
1970s, and mid-1980s (see Table 1).
Previous researchers attempted to link the occurrence
of JPBW outbreaks to weather conditions or climatic
variables. MacAloney (1944), for example, suggested that
droughty conditions might lead to JPBW outbreaks. Ives
(1981) evaluated relationships between weather variables
and the extent of JPBW defoliation in Manitoba and
Saskatchewan from 1937 to 1969. Ives found no strong associations, but speculated that extreme winter temperatures
could reduce survival of overwintering larvae and that
warm summer temperatures would be favorable for larval
development. When fire history was overlaid on a 50-year
time series of defoliation data from the same region, Volney
(1988) observed that years with large fires were followed 4–
7 years later by JPBW outbreaks. He suggested that fire
years were probably associated with droughty conditions,
and that unusually dry weather might have long-term
effects on JPBW or their host trees that would eventually
lead to high population densities.
Clancy et al. (1980) analyzed the first 17 years of the
JPBW population series collected annually in northwestern
Wisconsin to examine effects of weather on JPBW dynamics. Using forward stepping regression, they found that
several weather variables entered the models and explained
64%, 69%, and 62% of the variation observed in late-stage
larval counts, pupal counts, and defoliation, respectively.
Most of the variables included in the models reflected
departures from long-term precipitation or temperature
norms. Such a result might be expected, however, given that
JPBW population trends are in themselves departures from
long-term means. In addition, weather effects were not consistent among years and sometimes had opposing effects on
different life stages of JPBW.
Populations of other cyclic forest defoliators in North
America similarly exhibit spatial synchrony across wide
geographic areas (Myers 1998; Williams and Leibhold
1995). These patterns have been variously attributed to
regional climatic factors triggering population release
(Wellington et al. 1950), changes in host plant quality induced by regional drought (White 1978; Mattson and Haack
1987), entomopathogens (Myers 1993; Shepherd et al. 1988)
or dispersal among populations. It is difficult to test or
discount many of these factors, but Martinat (1987) noted
the low probability that weather patterns would exhibit
such regularity in timing and duration.
A more parsimonious explanation for the apparent
synchrony of many defoliator outbreaks, including those
of JPBW, may involve the Moran effect, a term coined by
Royama (1992) for Moran’s (1953) explanation of the
spatiotemporal synchrony of lynx dynamics across Canada.
The Moran effect suggests that a density-independent,
exogenous factor that is correlated across a region (such as
weather) can bring spatially discrete populations into
synchrony if the populations are locally regulated by a
similar density-dependent structure (Bjornstad et al. 1999;
Williams and Leibhold 1995). Moreover, time-lagged density dependence will increase the probability of synchrony
among populations (Hudson and Cattadori 1999). Unlike
251
Fig. 1. Areas defoliated during jack pine budworm outbreaks from 1937 to 1996 in the Canadian province of Ontario based on data recorded by
the Forest Insect and Disease Survey unit, Ontario region, of the Canadian Forest Service (Maps provided courtesy of A. Hopkin and R.
Fournier, Canadian Forest Service)
252
theories of climatic release, Moran effect processes require
no assumptions about the timing or regularity of weather
patterns or other exogenous factors, only that the exogenous factors be common among the populations.
Although an intensive spatiotemporal analysis of JPBW
dynamics is beyond the scope of this article, fluctuations of
JPBW populations appear generally consistent with Moran
effect processes, especially in the area encompassing the
Great Lakes states and Ontario. Lagged, density-dependent
processes have been identified in localized populations
(Volney and McCullough 1994; Nealis 1995) and could reflect increased mortality from late-instar larval parasitoids
and reduced production of pollen cones following heavy
defoliation. Specific exogenous factors that may be involved
in Moran effect dynamics are not known. Myers (1998)
found that outbreaks of several forest defoliators in North
America coincided with troughs in sunspot activity and
years with cool spring temperatures. On the other hand, low
water availability or droughty conditions have been frequently linked with increased JPBW density (MacAloney
1944; McCullough and Kulman 1991a; Volney 1988; Volney
and McCullough 1994).
The role that moth dispersal may play in the regional
fluctuations of JPBW populations is also of interest. Anecdotal reports suggest moth flight can be heavy during outbreaks (Michigan Dept. of Conservation 1965; Wisconsin
Dept. of Natural Resources 1994), potentially linking spatially disjunct populations (Bjornstad et al. 1999; Hudson
and Cattadori 1999). In addition, dispersal and Moran effect
processes are not mutually exclusive, but could operate at
different scales. For example, spatial synchrony of butterfly
populations appeared to reflect dispersal at a local scale
while the Moran effect dominated at a regional scale
(Sutcliffe et al. 1996; Hudson and Cattadori 1999). The
potential roles of dispersal or Moran effect processes on
JPBW population fluctuations warrant more intensive
analysis. An improved understanding of large-scale JPBW
dynamics could be helpful in predicting how shifts in distribution or fragmentation of jack pine forests, climate
change, or other perturbations may alter JPBW population
cycles.
Jack pine budworm and jack pine ecology
Although most research has addressed interactions between JPBW and individual trees or stand-level processes
during an outbreak, it is also useful to consider these interactions at larger spatial and temporal scales. In North
America, jack pine and lodgepole pine (Pinus contorta
Doug. Ex. Loud.) are the only pines in the boreal forest
(Critchfield 1985), and episodic outbreaks of insects play
important and similar roles in the ecology of both species.
Jack pine and lodgepole pine are well adapted to fire, and in
the absence of fire, these early successional species are generally replaced by more shade-tolerant species (Cayford
1970; Lotan and Critchfield 1990). As jack pine trees
age and annual growth rates slow, trees are more likely to
succumb to severe defoliation (Conway et al. 1999a;
McCullough et al. 1996; Volney 1998).
Over time, jack pine stands accumulate high fuel loads
because of tree mortality and topkill following JPBW outbreaks, along with other stresses. When fires ignite in jack
pine stands, they are often intense crown fires that consume
most standing trees and much of the woody debris and litter
on the forest floor (Cayford 1970; Heinselman 1973; Pyne
1984; Weber 1995). Serotinous cones open because of heat
generated by the fire and regeneration on exposed mineral
soil is often highly successful (Cayford 1970; Rudolph 1958).
Over time, the three-way relationship among jack pine,
JPBW, and fire perpetuates regeneration of jack pine,
ensuring the continued availability of hosts for JPBW
(McCullough et al. 1998; Nealis 1995; Weber 1995). Similarly, in the lodgepole pine ecosystem, mountain pine beetle
(Dendroctonus ponderosae Hopkins) preferentially attacks
large, old pines, again setting up conditions for intense fire
in senescing stands followed by regeneration of lodgepole
pine (Amman and Schmitz 1988; Stuart et al. 1989). In preEuropean settlement conditions, these interactions established age-class mosaics distributed across the landscape
(Cayford 1970; Heinselman 1973) and vulnerability to damage during outbreaks of pests such as JPBW similarly varied
at a landscape level. Fire suppression, design of harvest or
planting blocks, and other management decisions, therefore, can potentially influence JPBW dynamics across a
large geographic area (Kouki et al. 1997; McCullough et al.
1996; Radeloff et al. 2000; Volney 1988).
Jack pine expanded its range at a relatively rapid rate
following glaciation (Critchfield 1985). The resulting high
degree of genetic variability that occurs across the jack pine
range may influence interactions with JPBW or other pests.
For example, in the southern part of its range in the Great
Lakes region, jack pine trees produce both nonserotinous
and serotinous seed cones (Rudolph and Laidly 1990),
sometimes leading to uneven-aged, multistoried stands.
Understory or suppressed trees in these stands may intercept larvae dispersing from overstory trees, increasing survival of early-instar larvae (Batzer and Jennings 1980). In
its western range, jack pine hybridizes with lodgepole pine,
and resistance to four pests was positively correlated with
the degree of genetic introgression (Wu et al. 1996). Much
of the geographically ordered variation in jack pine occurs
in the Great Lakes region, reflecting early postglacial colonization of this area from a few refuges in eastern North
America (Critchfield 1985; Yeatman 1967). Seed sources
from Great Lakes states were found to vary considerably in
susceptibility to shoot-boring and sap-sucking insect pests,
but resistance to defoliators was not evaluated (Hodson
et al. 1982). Genetically different races of jack pine may
occur in four areas of the Great Lakes states and two areas
in Ontario, and one occurs in central Canada (Critchfield
1985). Another population may exist in eastern Canada
where the arrival of jack pine is most recent (Desponts and
Payette 1993). Processes affecting JPBW dynamics might be
expected to vary among these regions, but the general lack
of long-term JPBW population data has so far precluded
quantitative examination of these patterns.
253
Summary
Jack pine is a short-lived, seral species commonly found on
sandy soils with low moisture and nutrient availability. Jack
pine budworm is a native, univoltine insect that feeds preferentially on current-year foliage of jack pine, resulting in
reduced growth, topkill, and tree mortality. Outbreaks of
JPBW generally occur at cycles of 6–12 years and persist for
2–4 years across much of the jack pine range in the boreal
forest. Over time, interactive associations between JPBW
and fire result in regeneration of senescing jack pine stands
and ensure the continued availability of hosts for JPBW.
Although much of the biology of JPBW is well understood, more information is needed on aspects of its life cycle
and its interactions with host trees and natural enemies.
For example, anecdotal reports of moth flight and wide
variation in realized fecundity indicate that dispersal of
gravid moths may play a role in the spatial or temporal
dynamics of an outbreak. The frequency and extent of moth
dispersal and the factors that initiate moth flight have not
been examined.
Survival of early-instar larvae in spring is generally
closely associated with availability of pollen cones, which
provide a refuge for larvae until current-year foliage becomes available. Trees that have been severely defoliated,
however, produce few pollen cones the following year, resulting in increased dispersal and mortality of early-instar
larvae. Pollen cone production is highly variable and has
been related to tree vigor or availability of light, nitrogen,
and water. The physiological mechanisms that regulate
pollen cone formation are not well understood, limiting our
ability to develop predictive models.
Possible variation in susceptibility to JPBW defoliation
is suggested by the consistent presence of at least some
undefoliated trees in stands that are otherwise extensively
defoliated. Foliage quality may affect JPBW survival or
fecundity, but multigenerational studies will be needed to
identify causal mechanisms. Foliar nitrogen was related to
larval survival, although larvae can increase foliage consumption to compensate for low nitrogen levels. Monoterpenes are positively associated with foliar nitrogen but do
not appear to negatively affect JPBW survival, development, or fecundity. Site conditions, particularly moisture
availability, may be related to outbreak periodicity, but
whether this affects pollen cone production, secondary
compounds, or other aspects of host suitability is not
known.
Parasitism of early instars, especially by Apanteles
fumiferanae and Glypta fumiferanae, is frequently observed, although this mortality usually does not substantially affect JPBW population dynamics. Late instar and
pupal parasitism play a more important role in population
fluctuations. High rates of late-stage parasitism were associated with the collapse of JPBW outbreak populations
in separate studies in Michigan, Wisconsin, and Ontario,
although the specific parasitoids associated with this mortality varied regionally. The impact of predators is difficult to
assess, but in some situations, birds, ants, and other inverte-
brates may account for substantial larval mortality. Pathogens of JPBW remain relatively unexplored, although
microsporidia and a virus are known to affect larvae.
The scarcity of pollen cones on heavily defoliated trees
and increased parasitism of late-stage larvae and pupae
over the course of an outbreak are consistent with and may
account for the second-order, density-dependent factors
that were identified in a long-term population data set
from Wisconsin. These factors appear to operate in a similar
manner across much of the region inhabited by JPBW. Synchrony of some, albeit not all, JPBW outbreaks at a regional
scale may be indicative of Moran effect processes.
Although much has been learned about JPBW populations during outbreaks, we still understand relatively little
about the factors that maintain endemic JPBW populations
and what changes must occur to initiate an outbreak. Continued collection and analysis of population and defoliation data at scales ranging from individual trees to stands
to landscapes will provide information on multitrophic
interactions involving JPBW, its host and natural enemies,
as well as moth dispersal and Moran effect processes.
Potential influences of jack pine population genetics,
silvicultural activities, and natural disturbance on JPBW
dynamics have only begun to be explored (Kouki et al.
1997; Radeloff et al. 2000), and many interesting questions
remain. Such information will be useful in developing
mechanistic models of JPBW dynamics and improved
management recommendations to maintain healthy and
productive jack pine forests.
References
Alban DH, Perala DA, Schaegel BE (1978) Biomass and nutrient
distribution in aspen, pine, and spruce stands on the same soil type in
Minnesota. Can J For Res 8:290–299
Allen DC, Knight FB, Foltz JL, Mattson WJ (1969) Influence of
parasites on two populations of Choristoneura pinus (Lepidoptera:
Tortricidae) in Michigan. Ann Entomol Soc Am 62:1469–1475
Allen DC, Knight FB, Foltz JL (1970) Invertebrate predators of the
jack-pine budworm, Choristoneura pinus, in Michigan. Ann
Entomol Soc Am 63:59–64
Amman GD, Schmitz RF (1988) Mountain pine beetle-lodgepole pine
interactions and strategies for reducing tree losses. Ambio 17:62–
68
Batzer HO, Jennings DT (1980) Numerical analysis of a jack pine
budworm outbreak in various densities of jack pine. Environ
Entomol 9:514–524
Benjamin DM, Drooz AT (1954) Parasites affecting the jack-pine budworm in Michigan. J Econ Entomol 47:588–591
Bernard-Dagan C (1988) Seasonal variations in energy sources and
biosynthesis of terpenes in Maritime pine. In: Mattson WJ, Levieus
J, Bernard-Dagan C (eds) Mechanisms of woody plant defenses
against insects. Springer-Verlag, New York, pp 93–116
Bjørnstad ON, Ims RA, Lambin X (1999) Spatial population dynamics:
analyzing patterns and processes of population synchrony. Trends
Ecol Evol 14:427–432
Brandt NR, Melvin JCE (1970) Parasites of the jack-pine budworm,
Choristoneura pinus pinus Free., in Manitoba, Saskatchewan and
northwestern Ontario. For Res Lab Rep MS-X-29. Canadian Forest
Service, Department of Fisheries and Forestry, Winnipeg
Campbell IM (1953) Morphological differences between the pupae
and the egg clusters of Choristonuera fumiferana (Clem.) and C.
pinus Free. (Lepidoptera: Tortricidae). Can Entomol 85:134–135
254
Campbell RW (1993) Population dynamics of the major North American needle-eating budworms. Res Pap PNW-RP-463. USDA Forest
Service, Pacific Northwest Research Station, Portland, OR
Cates RG, Henderson CB, Redak RA (1987) Responses of the western
spruce budworm to varying levels of nitrogen and terpenes.
Oecologia (Berl) 73:312–316
Cayford JH (1970) The role of fire in the ecology and silviculture of
jack pine. In: Proceedings, 10th annual tall timbers fire ecology conference, Tall Timbers Research Station, Tallahassee, pp 221–244
Clancy KM, Giese RL, Benjamin DM (1980) Predicting jack-pine budworm infestations in northwestern Wisconsin. Environ Entomol
9:743–751
Conway BE, Leefers LA, McCullough DG (1999a) Financial evaluation of a jack pine budworm outbreak and implications for management. Can J For Res 29:382–392
Conway BE, McCullough DG, Leefers LA (1999b) Effects of multiple
jack pine budworm outbreaks on the growth of jack pine trees in
Michigan. Can J For Res 29:1510–1517
Critchfield WB (1985) The late Quaternary history of lodgepole and
jack pine. Can J For Res 15:749–772
Desponts M, Payette S (1993) The Holocene dynamics of jack pine at
its northern range limit in Quebec. J Ecol 81:719–727
Dixon JC, Benjamin DM (1963) Natural control factors associated with
the jack-pine budworm, Choristoneura pinus. J Econ Entomol
56:266–270
Drooz AT, Benjamin DM (1956) Parasites from two jack-pine budworm outbreaks on the upper peninsula of Michigan. J Econ
Entomol 49:412–413
Elliott NC, Simmons GA, Chilcote C (1986) Parasitism of early
instar jack pine budworm (Lepidoptera: Tortricidae) by Apanteles
spp. (Hymenoptera: Braconidae) and Glypta fumiferanae
(Hymenoptera: Ichneumonidae). Great Lakes Entomol 19:67–72
Foltz JL, Knight FB, Allen DC (1972) Numerical analysis of population fluctuations of the jack pine budworm. Ann Entomol Soc Am
65:82–89
Foster NW, Morrison IK (1976) Distribution and cycling of nutrients in
a natural Pinus banksiana ecosystem. Ecology 57:110–120
Fowler GW, Simmons GA (1987) Regression equations and table for
estimating numbers of eggs in jack pine budworm (Lepidoptera:
Tortricidae) egg masses in Michigan. Great Lakes Entomol 201:157–
160
Freeman TN (1953) The spruce budworm Choristoneura fumiferana
(Clem.) and an allied new species on pine (Lepidoptera:
Tortricidae). Can Entomol 85:121–127
Freeman TN (1967) On coniferophagous species of Choristoneura
(Lepidoptera: Tortricidae) in North America. Can Entomol 99:449–
455
Gershenzon J (1984) Changes in the levels of plant secondary metabolites under water and nutrient stress. Recent Adv Phytochem 18:273–
320
Graham SA (1935) The spruce budworm on Michigan pine. Bull no 6,
University of Michigan, School of Forestry and Conservation, Ann
Arbor, MI
Grant GG, Langevin D (1994) Oviposition responses of four
Choristoneura (Lepidoptera: Tortricidae) species to chemical and
physical stimuli associated with host and nonhost foliage. Environ
Entomol 23:447–456
Greenbank DO (1957) The role of climate and dispersal in the initiation of outbreaks of the spruce budworm in New Brunswick. II. The
role of dispersal. Can J Zool 35:385–403
Greenbank DO, Schaefer GW, Rainey RC (1980) Spruce budworm
(Lepidoptera: Tortricidae) moth flight and dispersal: new understanding from canopy observations, radar and aircraft. Mem
Entomol Soc Canada 110:1, 85, 120–123, 150
Gross HL (1992) Impact analysis for a jack pine budworm infestation
in Ontario. Can J For Res 22:818–831
Gross HL, Meating JH (1994) Impact of the 1982–1986 jack pine
budworm infestation on jack pine in northeastern Ontario. Info Rep
O-X-431, Canadian Forest Service, Great Lakes Forestry Centre,
Sault Ste. Marie, Ontario
Hansen RW (1988) Phenological and nutritional interactions between
the jack pine budworm and jack pine, and sampling early instars of
the jack pine budworm. PhD thesis, Department of Entomology,
University of Minnesota, St. Paul, MN
Harcomb PA (1987) Tree life tables. BioScience 37:550–556
Harrison DLS, Owens JN (1992) Gibberellin A4/7 enhanced cone
production in Tsuga heterophylla: the influence of gibberellin A4/7
on seed- and pollen-cone production. Int J Plant Sci 153:171–177
Harvey GT (1985) The taxonomy of coniferophagous Choristoneura
(Lepidoptera: Tortricidae): a review. In: Sanders CJ, Stark RW,
Mullins EJ, Murphy J (eds) Recent advances in spruce budworm
research. Proceedings of the CANUSA spruce budworms research
symposium, September 1984, Bangor, Maine. Canadian Forestry
Service, Ottawa, pp 16–59
Harvey GT (1996) Genetic relationships among Choristoneura species
(Lepidoptera: Tortricidae) in North America as revealed by isozyme
studies. Can Entomol 128:245–262
Heinselman ML (1973) Fire in the virgin forests of the Boundary
Waters Canoe Area. Minn Quat Res 3:329–382
Hodson AC, Zehngraff PJ (1946) Budworm control in jack pine by
forest management. J For 44:198–200
Hodson AC, French DW, Jensen RA, Bartelt RJ (1982) The susceptibility of jack pine from Lake States seed sources to insects and
diseases. Res Pap NC-225, USDA Forestry Service, North Central
Forestry Experimental Station, St. Paul, MN
Howse G, Meating J (1995) Jack pine budworm situation in Ontario
1986–1994. In: Volney WJA, Nealis VG, Howse GM, Westwood
AR, McCullough DG, Laishley BL (eds) Jack pine budworm biology and management. Proceedings of the jack pine budworm
Symposium, January 24–26, 1995, Winnipeg, Manitoba. Info Rep
NOR-X-342, Canadian Forest Service, Northwest Region,
Edmonton, Alberta pp 31–34
Hudson PJ, Cattadori IM (1999) The Moran effect: a cause of population synchrony. Trends Ecol Evol 14:1–2
Innes DGL, Bendell JF, Naylor BJ, Smith BA (1990) High densities of
the masked shrew, Sorex cinereus, in jack pine plantations in northern Ontario. Am Midl Nat 124:330–341
Ives WGH (1981) Environmental factors affecting 21 forest insect
defoliators in Manitoba and Saskatchewan, 1945–69. Info Rep NORX-233, Canadian Forestry Service, Northern Forestry Research Center, Edmonton, Alberta
Jennings DT (1971) Ants preying on dislodged jack-pine budworm
larvae. Ann Entomol Soc Am 64:384–385
Johnson SA (1968) Biotic environmental effects on the fecundity of
jack pine budworm. MF thesis, University of Michigan, Ann Arbor,
MI
Jones AC, Campbell J (1986) Jack pine budworm: the Minnesota situation. In: Jack pine budworm information exchange, January 1986,
Winnipeg, pp 7–9
Kotar J, Kovach JA, Locey CT (1988) Field guide to forest habitat
types of northern Wisconsin. Department of Forestry, University
of Wisconsin-Madison and Wisconsin Department of Natural
Resources, Madison
Kouki J, McCullough DG, Marshall LD (1997) Effects of forest stand
and edge characteristics on the vulnerability of jack pine stands to
jack pine budworm (Choristoneura pinus pinus) (Lep., Tortricidae)
damage. Can J For Res 27:1765–1772
Kulman HM, Hodson AC (1961a) The jack-pine budworm as a pest of
other conifers with special reference to red pine. J Econ Entomol
54:1221–1224
Kulman HM, Hodson AC (1961b) Feeding and oviposition habits of
the jack-pine budworm. J Econ Entomol 54:1138–1140
Kulman HM, Hodson AC (1961c) Parasites of the jack-pine budworm,
Choristoneura pinus, with special reference to parasitism at particular stand locations. J Econ Entomol 54:221–224
Kulman HM, Hodson AC (1962) A sampling unit for the jackpine budworm Choristoneura pinus. J Econ Entomol 55:801–802
Kulman HM, Hodson AC, Duncan DP (1963) Distribution and effects
of jack pine budworm defoliation. For Sci 9:146–157
LeJeune RR (1950) The effect of jack-pine staminate flowers on
the size of larvae of the jack-pine budworm, Choristoneura sp. Can
Entomol 82:34–43
LeJeune RR, Black WF (1950) Population of larvae of the jack-pine
budworm. For Chron 26:152–156
Lomic PV, Nealis VG (1996) Behaviour of jack pine budworm
(Lepidoptera: Tortricidae) on vegetative or pollen-cone shoots. Proc
Entomol Soc Ont 127:63–66
Lotan JE, Critchfield WB (1990) Pinus contorta Dougl. Ex. Loud. In:
Silvics of North America, vol 1, Conifers. Agric Handbook 654.
USDA, Forest Service, Washington, DC, pp 302–315
255
Lysyk TJ (1989) A multiple-cohort model for simulating jack pine
budworm (Lepidoptera: Tortricidae) development under variable
temperature conditions. Can Entomol 121:373–387
MacAloney HJ (1944) Relation of root condition, weather, and insects
to the management of jack pine. J For 42:124–139
Martinat PJ (1987) The role of climatic variation and weather in forest
insect outbreaks. In: Barbosa P, Schultz J (eds) Insect outbreaks.
Academic Press, New York, pp 241–268
Mattson WJ (1980) Herbivory in relation to plant nitrogen content.
Annu Rev Ecol Syst 11:119–161
Mattson WJ, Haack RA (1987) The role of drought in outbreaks of
plant-eating insects. BioScience 37:110–118
Mattson WJ, Knight FB, Allen DC, Foltz JL (1968) Vertebrate predation on the jack-pine budworm in Michigan. J Econ Entomol 61:229–
234
McCullough DG, Kulman HM (1991a) Differences in foliage quality of
young jack pine (Pinus banksiana Lamb.) on burned and clearcut
sites: effects on jack pine budworm (Choristoneura pinus pinus Freeman). Oecologia (Berl) 98:135–145
McCullough DG, Kulman HM (1991b) Effects of nitrogen fertilization
on young jack pine (Pinus banksiana Lamb.) and on its suitability
as a host for jack pine budworm (Choristoneura pinus pinus) (Lepidoptera: Tortricidae). Can J For Res 21:1447–1458
McCullough DG, Swedenborg PD, Kulman HM (1993) Effects of nitrogen fertilization on monoterpenes of jack pine seedlings and
weight gain of jack pine budworm (Lepidoptera: Tortricidae). Great
Lakes Entomol 26:137–149
McCullough DG, Katovich S, Heyd RL, Weber S (1994) How to manage jack pine budworm. For Pest Leaf NA-FR-01-94, USDA Forest
Service, St. Paul, MN
McCullough DG, Marshall LD, Buss L, Kouki J (1996) Relating jack
pine budworm damage to stand attributes in northern Michigan. Can
J For Res 26:2180–2190
McCullough DG, Werner RA, Neumann D (1998) Fire and insects in
northern and boreal forests of North America. Annu Rev Entomol
43:107–127
Michigan Dept. of Conservation (1965) Forest pest report: 1965. Michigan Department of Conservation, Lansing, MI
Miller WE (1987) Spruce budworm (Lepidoptera: Tortricidae): role
of adult imbibing in reproduction. Environ Entomol 16:1291–1295
Moody BH (1986) The jack pine budworm – history of outbreaks,
damage and FIDS sampling and prediction systems in the Prairie
Provinces. In: Jack pine budworm information exchange, January
1986, Winnipeg, pp 15–22
Moran PAP (1953) The statistical analysis of the Canadian lynx cycle.
II. Synchronization and meteorology. Aust J Zool 1:291–298
Muzika RM, Pregitzer KS, Hanover JW (1989) Changes in terpene
production following nitrogen fertilization of grand fir (Abies
grandis (Dougl.) (Lindl.) seedlings. Oecologia (Berl) 80:485–489
Myers JH (1993) Population outbreaks in forest Lepidoptera. Am Sci
81:240–251
Myers JH (1998) Synchrony in outbreaks of forest Lepidoptera: a
possible example of the Moran effect. Ecology 79:1111–1117
Nealis VG (1987) The number of instars in jack pine budworm,
Choristoneura pinus pinus Free. (Lepidoptera: Tortricidae), and the
effect of parasitism on head capsule width and development time.
Can Entomol 119:773–777
Nealis VG (1991) Parasitism in sustained and collapsing populations
of the jack pine budworm, Choristoneura pinus pinus Free. (Lepidoptera: Tortricidae) in Ontario, 1985–1987. Can Entomol 123:1065–
1075
Nealis VG (1995) Population biology of the jack pine budworm. In:
Volney WJA, Nealis VG, Howse GM, Westwood AR, McCullough
DG, Laishley BL (eds) Jack pine budworm biology and management. Proceedings of the jack pine budworm symposium, January
24–26, 1995, Winnipeg, Manitoba. Northwest Region Info Rep
NOR-X-342, Canadian Forestry Service, Edmonton, Alberta, pp 55–
72
Nealis VG, Lomic PV (1994) Host-plant influence on the population
ecology of the jack pine budworm (Choristoneura pinus) (Lepidoptera: Tortricidae). Ecol Entomol 19:367–373
Nealis VG, Lysyk TJ (1988) Sampling overwintering jack pine budworm, Choristoneura pinus pinus Free. (Lepidoptera: Tortricidae)
and two of its parasitoids (Hymenoptera). Can Entomol 120:1101–
1111
Nealis VG, Lomic PV, Meating JH (1997) Forecasting defoliation by
the jack pine budworm. Can J For Res 27:1154–1158
Pyne SJ (1984) Introduction to wildland fire. Wiley, New York
Radeloff VC, Mladenoff DJ, Boyce MS (2000) Effects of interacting
disturbances on landscape patterns: budworm defoliation and salvage logging. Ecol Appl 10:233–247
Royama T (1992) Analytical population dynamics. Chapman & Hall,
London
Rudolf PO (1958) Silvical characteristics of jack pine. Pap 61. USDA
Forest Service, Lake States Forestry Experimental Station, St. Paul,
MN
Rudolph TD, Laidly PR (1990) Jack pine. In: Silvics of North America,
vol 1, Conifers. Agric Handbook 654. USDA Forest Service, Washington, DC, pp 280–293
Sanders CJ (1971) Daily activity patterns and sex pheromone specificity as sexual isolating mechanisms in two species of Choristoneura
(Lepidoptera: Tortricidae). Can Entomol 103:498–502
Sanders CJ, Lucuik GS (1975) Effects of photoperiod and size on flight
activity and oviposition in the eastern spruce budworm (Lepidoptera: Tortricidae). Can Entomol 107:1289–1299
Scarr T (1995) Phenotypic variation in jack pine susceptibility to jack
pine budworm. In: Volney WJA, Nealis VG, Howse GM, Westwood
AR, McCullough DG, Laishley BL (eds) Jack pine budworm biology and management. Proceedings of the jack pine budworm symposium, January 24–26, 1995, Winnipeg, Manitoba Northwest Region
Info Rep NOR-X-342, Canadian Forestry Service, Edmonton,
Alberta, pp 79–88
Shepherd RF, Bennett DD, Dale JW, Tunnock S, Dolph RE, Thier
RW (1988) Evidence of synchronized cycles in outbreak patterns of
Douglas-fir tussock moth, Orygia pseudotsugata. Mem Entomol Soc
Can 146:107–121
Silk PJ, Kuenen LPS (1988) Sex pheromones and behavioral biology
of the coniferophagous Choristoneura. Annu Rev Entomol 33:83–
101
Simmons GA, Sloan NF (1974) Consumption of jack pine budworm
Choristoneura pinus Freeman, by the eastern chipping sparrow,
Spizella passerina (Bechstein). Can J Zool 52:817–821
Sloan NF, Simmons GA (1973) Foraging behavior of the chipping
sparrow in response to high populations of jack pine budworm. Am
Midl Nat 90:210–215
Sperling FAH, Hickey DA (1995) Amplified mitochondrial DNA as
a diagnostic marker for species of conifer-feeding Choristoneura
(Lepidoptera: Tortricidae). Can Entomol 127:277–288
Stairs GR (1960) Infection of the jack pine budworm, Choristoneura
pinus Freeman, with a nuclear polyhedrosis virus of the spruce
budworm, Choristoneura fumiferana (Clemens), (Lepidoptera:
Tortricidae). Can Entomol 92:906–908
Stuart JD, Agee JK, Gara RI (1989) Lodgepole pine regeneration in an
old, self-perpetuating forest in south Oregon. Can J For Res
19:1096–1104
Sutcliffe OL, Thomas CD, Moss D (1996) Spatial synchrony and
asynchrony in butterfly population dynamics. J Anim Ecol 65:85–95
Thomson HM (1959) A microsporidian infection in the jack-pine
budworm, Choristoneura pinus Free. Can J Zool 37:117–120
Turchin P (1990) Rarity of density dependence or population regulation with lags? Nature (Lond) 344:660–663
Volney WJA (1988) Analysis of historic jack pine budworm outbreaks
in the Prairie provinces of Canada. Can J For Res 18:1152–1158
Volney WJA (1989) Biology and dynamics of North American
coniferophagous Choristoneura populations. Agric Zool Rev 3:133–
156
Volney WJA (1998) Ten-year tree mortality following a jack pine
budworm outbreak in Saskatchewan. Can J For Res 28:1784–1793
Volney WJA, McCullough DG (1994) Jack pine budworm population
behaviour in northwestern Wisconsin. Can J For Res 24:502–510
Wallin KF, Raffa DF (1998) Association of within-tree jack pine budworm feeding patterns with canopy level and within-needle variation
of water, nutrient, and monoterpene concentrations. Can J For Res
28:228–233
Weber SD (1986) Jack pine management. In: Proceedings jack pine
budworm information exchange. Manitoba Department of Natural
Resources, Winnipeg, Manitoba, January 1986, pp 12–14
Weber S (1995) Integrating budworm into jack pine silviculture in
northwest Wisconsin. In: Volney WJA, Nealis VG, Howse GM,
Westwood AR, McCullough DG, Laishley BL (eds) Jack pine bud-
256
worm biology and management. Proceedings of the jack pine budworm symposium, January 24–26, 1995, Winnipeg, Manitoba. Northwest Region Info Rep NOR-X-342, Canadian Forest Service,
Edmonton, Alberta pp 19–24
Wellington WG, Fettes JJ, Turner KB, Belyea RM (1950) Physical and
biological indicators of the development of outbreaks of the spruce
budworm, Choristoneura fumiferana (Clem.). Can J Res Sect D Zool
Sci 28:308–331
Wisconsin Dept. of Natural Resources (1994) Forest health conditions
in Wisconsin: annual report. Forest Health Protection Unit, Wisconsin Department of Natural Resources, Madison, WI
White TCR (1978) The importance of a relative shortage of food in
animal ecology. Oecologia (Berl) 33:71–86
Wilde SA, Iyer JG, Tanzer C, Trautmann WL, Watterston KG
(1964) Growth of jack pine (Pinus banksiana Lamb.) plantations
in relation to fertility of non-phreatic sandy soils. Soil Sci 98:162–
169
Williams DW, Leibhold AM (1995) Influence of weather on the
synchrony of gypsy moth (Lepidoptera: Lymantriidae) outbreaks
in New England. Environ Entomol 24:987–995
Wilson GG (1986) A comparison of the effects of Nosema fumiferanae
and a Nosema sp. (microsporida) on Choristoneura fumiferana
(Clem.) and Choristoneura pinus pinus Free. Info Rep FPM-X-77,
Canadian Forestry Service, Forest Pest Management Institute, Sault
Ste. Marie, Ontario
Wu HX, Ying CC, Muir JA (1996) Effect of geographic variation and
jack pine introgression on disease and insect resistance in lodgepole
pine. Can J For Res 26:711–726
Yeatman CW (1967) Biogeography of jack pine. Can J Bot 45:2201–
2211