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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 244 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 245 (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 246 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. 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