Abstract
One of the most significant categories of insect that cause damage to trees are the defoliators. While many orders of insects feed on tree foliage, in this chapter we will focus on Lepidoptera, as there are so many Lepidopteran larvae (caterpillars) that are known for their extensive tree damage. In this chapter we review the impact of foliage feeders on forest trees and stand composition, and the ways in which densities of these species or the defoliation they cause are monitored. We do not cover insects attacking ornamental trees in the landscape, nor do we cover insects feeding exclusively on foliage tips or buds.
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9.1 Introduction
One of the most significant categories of insects that cause damage to trees are the defoliators. While many orders of insects feed on tree foliage, in this chapter we will focus on Lepidoptera, as there are so many Lepidopter larvae (caterpillars) that are known for their extensive tree damage. In this chapter we review the impact of foliage feeders on forest trees and stand composition, and the ways in which densities of these species or the defoliation they cause are monitored. We do not cover insects attacking ornamental trees in the landscape, nor do we cover insects feeding exclusively on foliage tips or buds. The species we include live and feed externally on the leaves and remove or consume leaf tissue that may or may not include leaf veins. Other species, called leaf miners, live and feed as larvae between the upper and lower surface of the leaf and produce characteristic patterns of leaf damage. Most of those species are considered pests of ornamental trees and are not included in this chapter. We provide more detail on two key species as case studies: winter moth, Operophtera brumata L, and spongy moth, Lymantria dispar L. These species are two of the most widely studied of all foliage-feeding insects attacking forest trees. Treatment of other important species such as spruce budworm, Choristoneura fumiferana, would produce a chapter too long for the current volume. That species, and others like it, are included in a table (Table 9.1) of the world’s most forest-damaging Lepidoptera and Hymenoptera, along with key references that provide access to the most recent and important literature.
9.2 Effects of Defoliation on Forest Trees
The general public often views defoliation in terms of aesthetics and potential economic effects. Beyond simply affecting the growth and life of the defoliated trees, defoliation has many indirect effects that have implications for future defoliator population dynamics and forest nutrient cycling, in turn affecting overall forest composition.
Defoliation that removes some or all of the leaf canopy of trees has a large impact on the ability of trees to produce carbohydrates, and most studies have shown foliage loss to be directly proportional to reductions in tree growth. While defoliation can cause tree mortality, this often occurs indirectly, as defoliation increases the susceptibility of trees to secondary insects and disease, which then are the ultimate cause of tree mortality (Kulman 1971). Outbreaks of defoliators are major events in forests worldwide and may produce landscape-wide patterns of tree mortality and result in major changes in stand tree species composition.
Even if there is no current folivore outbreak, trees may still be suffering the effects of past defoliation events. For instance, a study done in Cerro Castillo National Park by Piper, Gundale and Fajardo (2015) on Nothofagus pumilio, a South American deciduous tree, found that natural defoliation by Ormiscodes amphimone (Saturniidae) did not cause tree mortality. However, defoliated trees showed significantly stunted growth in comparison to non-defoliated trees. Contrary to previous assumptions, this growth limitation could not be explained by limitations in C and N availability. Defoliation by the larvae of the invasive winter moth (Operophtera brumata L.) has been shown to cause a significant reduction in radial growth and latewood production of Quercus trees in the same year as defoliation, as well as a reduction in earlywood production the subsequent year (Simmons et al. 2014).
Many trees produce defensive compounds in their leaves, such as phenolics or tannins, to defend themselves against free-feeding insects (Feeny 1970). On the other hand, many foliage-feeding insects are well adapted to cope with these compounds in their diet. There exists a very large literature dealing with the mode of action of tannin or phenolic compounds on insect performance, and whether or not trees respond to defoliation by producing more defensive compounds (Salminen and Karonen 2011).
When it comes to tree resistance to defoliators, there are two main types of resistance: constitutive (always present) and induced (as the result of defoliation). These effects may be either direct, wherein the plant produces either mechanical or molecular herbivore deterrents, or indirect, whereby they put up defenses, chemical or otherwise, that attract defoliator predators or parasitoids (War et al. 2012).
An important molecular mechanism plants use for defoliation resistance is the production of phenolic compounds, such as tannins, which include hydrolysable tannins, proanthocyanidins, and phlorotannins. Different kinds of tannins have greater impacts on different types of herbivores. In insects, different parts of the digestive system have different pH levels, and, as a result, differently structured tannins will react and metabolize differently in different sections of the gut, as they are hydrolyzed or oxidized. Rather than tannins themselves, it is possible that tannin metabolites are what actually affect herbivores (Salminen and Karonen 2011).
Tannins may serve as an important factor in tree constitutive resistance. Although some herbivore species have adapted to feed on certain tannins, for non-adapted defoliators they can serve as a feeding deterrent. Tannins may also be important for induced defenses, as multiple studies have shown tannin production increases with insect damage. However, there are many other factors at play, and tannin concentration is affected by things such as environmental stress. There are so many different specific types of tannins produced by plants and so many potential interactions that most current studies are correlative rather than causative (Barbehenn and Constabel 2011). For instance, there have been disparate findings on the relationship between tannin content and amount of defoliation. A recent study on spongy moth defoliation on Quercus ilex found no relationship (Solla et al. 2016).
Haukioja (1991) reviewed studies on tree-induced resistance to insect defoliation. While in general insect growth rate declined with decreased food quality, there were very mixed results about the effect of induced responses. Some studies showed that foliage damage induced changes in present and future leaves that were detrimental to insects, while others showed no effect of induced resistance. To complicate matters, other studies mentioned in the review showed improved performance of insects that fed on defoliated trees. Haukioja’s review made an important distinction between rapid and delayed induced resistance. The latter refers to changes in foliage chemistry that persist one or more years beyond the defoliation event, rather than those immediately following the defoliation in the same year. Only delayed induced resistance can cause the delayed density-dependent responses (see Chapter 7) that might cause forest insects to exhibit population cycles. Such effects have been proposed for autumnal moth (Haukioja 1991) and for larch budmoth (see Chapter 7; Baltensweiler and Fischlin 1988). In many cases it is not clear whether the changes in foliage chemistry involve defensive compounds or delayed effects on foliage that affect their nutrient quality.
White spruce (Picea glauca) trees resistant to defoliation by spruce budworm had different phenolic compounds present than non-resistant trees. Those phenolic compounds present in resistant trees were found to reduce fitness of spruce budworms (Delvas et al. 2011). However, as shown in a recent study, spruce budworm (Choristoneura fumiferana (Clem.)) that fed on resistant white spruce trees (Picea glauca (Moench) Voss) had greater fitness than those that fed on susceptible trees (Quezada-Garcia et al. 2015). Hodar et al. (2015) found that the chemical defenses in three species of pine were constitutive rather than induced. Several important herbivores are undeterred by these defenses, such as the pine processionary moth (Thaumetopoea pityocampa). Ultimately, as summarized by War et al. (2012), there is still much work needed to understand the biochemical response of induced resistance and how it is invoked by insect feeding.
9.3 Monitoring for Defoliation and Changes in Defoliator Population Densities
Defoliation has typically been mapped by aerial survey. For example, aerial maps of spruce budworm outbreaks have long been produced by the Canadian Forest Service (Fig. 9.1a). Annual defoliation maps of spongy moth in the eastern United States have been analyzed extensively to detect multi-annual cycles and spatial synchrony of spongy moth populations (Liebhold et al. 2004; Johnson et al. 2006b; Bjørnstad et al. 2008, 2010; Haynes et al. 2013, 2018a). Elkinton et al. (2014) used aerial survey maps of winter moth defoliation to estimate rates of spread of winter moth in the northeastern United States. More recently, imagery obtained from satellites or other forms of remote sensing has been used to map and analyze the expansion of defoliator outbreaks. Pasquarella et al. (2018) used Landsat imagery to portray the extent, severity and spread of spongy moth outbreak in the northeastern United States (Fig. 9.1b). Jepsen et al. (2009a) analyzed MODIS satellite data to relate winter moth defoliation to the timing of spring bud-burst in northern Fennoscandia. See reviews by Hall et al. (2006) and Chapter 19 for more detailed discussion of this topic.
Pheromone traps have often been used to map the spread of invasive species on the landscape. For example, Elkinton et al. (2010) used pheromone-baited traps to monitor the extent of the new invasion of winter moth in the northeastern United States (Fig. 9.2a) and its subsequent spatial spread (Elkinton et al. 2014). By far the most extensive use of pheromone traps anywhere in the world has been the Slow the Spread Program (Tobin and Blackburn 2007) to monitor the spread of spongy moth (Fig. 9.2b). Each year more than 100,000 traps are deployed along this invasion front. Pheromone traps are less frequently used to monitor changes in density of outbreak species in regions where they are native or widely established because such traps often fill to capacity even in low-density populations. Therefore, it is more common to use sampling of other life stages, such as egg mass counts for spongy moth, to measure changes in population density. See Chapter 19 for a more thorough discussion of this topic.
9.4 Case Study 1: Winter Moth
9.4.1 Biology and Host Range
The winter moth, Operophtera brumata L, is a geometrid species that is native to Europe, where it is one of the most common Lepidoptera feeding on a wide range of tree species. These include oaks (Quercus), maples (Acer), birches (Betula) and many others (Wint 1983). It is an occasional orchard pest, because it performs extremely well on apple (Malus). It is also especially damaging to blueberry (Vaccinium) crops, because the larvae feed inside the buds, where they are inaccessible to most pesticides and destroy developing berries before the buds open. In Europe, outbreaks of winter moth have occurred on Sitka spruce (Picea sitchensis) (Stoakley 1985; Watt and Mcfarlane 1991), on heather (Calluna vulgaris) in Scotland (Kerslake et al. 1996), and on mountain birch (Betula pubescens czereapanovii) in Fennoscandia (Jepsen et al. 2008).
Winter moth gets its name from the fact that adults typically emerge in November or December. The females attract males with a pheromone (Roelofs et al. 1982) and, after mating, lay eggs singly on the bark of host trees and overwinter in this stage. Winter moth larvae typically hatch at or before budbreak of their host trees and then bore into the expanding buds, so much of the damage occurs before leaf expansion. Classic work by Feeny (1970) proposed that winter moth is one of a suite of early spring-feeding Lepidoptera larvae that are relatively intolerant to accumulated tannins in oak foliage. Even though there may be many larvae per bud in outbreak populations, defoliation of oak and maple in New England, at least, rarely approaches 100%, presumably because the larvae finish feeding and pupate before defoliation is complete. Given that pupation occurs before the end of May, Pepi et al. (2016) showed that winter moth larvae disperse from partially defoliated oak leaves, possibly in response to tannins or other compounds induced by defoliation. Although the typical damage caused by winter moth results in only partially defoliated leaves, this can cause lasting damage to the tree, especially when defoliation persists year after year, as it did in Nova Scotia in the 1950s (Embree 1965, 1967) and Massachusetts after 2004 (Elkinton et al. 2014). Simmons et al. (2014) showed that defoliation by winter moth caused significant decline in tree growth in red oak (Quercus rubra L.) in Massachusetts, as measured by growth rings in increment cores of tree stems. Embree (1967) reported that repeated defoliation by winter moth resulted in as much as 40% tree mortality in red oak stands in Nova Scotia.
9.4.2 Geographical Range
Winter moth occurs in every European country, as well as Iran and Tunisia. Early reports included the Russian Far East and Japan, but the Japanese population was redescribed as Operophtera brunnea (Nakajima 1991). Recent collections from the Russian Far East suggest that those populations also are closely related to O. brunnea (Andersen et al. unpublished). Winter moth has been introduced to four distinct locations in North America: Nova Scotia in the 1930s (Hawboldt and Cuming 1950), Oregon in the 1950s (Kimberling et al. 1986), the region around Vancouver, British Columbia in the 1970s (Gillespie et al. 1978) and in the northeastern United States in the 1990s (Elkinton et al. 2010). Recent studies of winter moth DNA (microsatellites) from these populations by Andersen et al. (2021a) indicate that all four populations represent separate introductions from different European sources. The same techniques show that European populations of winter moth arose from distinct eastern and western forested glacial refugia that existed at the height of the last Ice Age 20,000 years ago (Andersen et al. 2017). Molecular analyses also have shown that in North America winter moth readily hybridizes with a native congener Bruce spanworm, O. bruceata, (Elkinton et al. 2010; Havill et al. 2017), that hybridization occurs in all regions where winter moth is known to have invaded (Andersen et al. 2019a), and that, at least in the northeastern United States, the hybrid zone appears to be stable in nature, existing under a tension hybrid zone model (Andersen et al. 2022).
9.4.3 Early Ecological Studies
Winter moth is one of the most famous of all forest insects, due in large part to the classic work by Varley and Gradwell (1960, 1963, 1968, 1970) and Varley et al. (1973), who collected annual life table data on this species on four oak trees near Oxford University in England during the 1950s and 1960s. They introduced important methodology for collecting annual data on density and mortality of different life stages and how to analyze the data to detect the presence of density-dependent factors regulating density and the causes of year-to-year changes in density. Based on these studies, they concluded that winter moth densities were typically regulated at low density by a community of predators that preyed upon winter moth pupae in the leaf litter beneath the infested trees. Subsequent research suggested that pupal predation was caused mainly by staphylinid and carabid beetles (Frank 1967). Other sources of mortality, including overwintering mortality and larval mortality combined, were not density-dependent, but experienced large year-to-year variation in impact and were thus responsible for the observed changes in population density. Varley and Gradwell used the term ‘key factor’ to describe such mortality factors.
Varley and Gradwell (1960, 1968) believed that the main cause of overwintering mortality was the periodic failure of winter moth hatch to adequately synchronize with budburst of their principal host trees, mainly oaks (Quercus). These ideas have been supported by research in North America (Embree 1965) and by Jepsen et al. (2009b), who studied outbreaks of winter moth in northern Fennoscandia.
9.4.4 Pathogens
Like most outbreak species of forest Lepidoptera, winter moth larvae are killed by a nuclear polyhedrosis virus (NPV) (Wigley 1976; Raymond et al. 2002; Raymond and Hails 2007). This virus has been recovered from winter moth in North America (Burand et al. 2011; Broadley et al. 2017), but it rarely, if ever, causes a major epizootic resulting in the collapse of outbreak populations. The virus is thus different from those that occur in other forest Lepidoptera such as spongy moth, Lymantria dispar, (Campbell and Podgwaite 1971) or forest tent caterpillar, Malacosoma disstria (Cooper et al. 2003), whose outbreaks are typically terminated by these agents. Broadley et al. (2017) showed that the NPV of winter moth was closely related to, but distinct from, an NPV recovered from Bruce spanworm (O. bruceata), the North American congener of winter moth. These two NPV’s were not cross-infective in the other species, discounting an earlier suggestion (Murdoch et al. 1985) that declines of winter moth in Nova Scotia in the 1950s might have been partially caused by infection of winter moth populations with viruses derived from Bruce spanworm.
Microsporidia are another pathogen that have been recovered from winter moth in Europe (Canning 1960; Canning et al. 1983) and were recorded by Varley et al. (1973). Broadley (2018) showed that microsporidia in North America (Donahue et al. 2019) were a major source of mortality in the rare outbreak populations of the North American congener of winter moth, Bruce spanworm, O. bruceata. They have not been recovered from winter moth in North America (Broadley 2018).
9.4.5 Biological Control in North America
Winter moth invaded Nova Scotia in Canada sometime before 1930 and soon caused widespread defoliation of oak forests in that region (Hawboldt and Cuming 1950). Beginning in 1954, Embree and colleagues undertook what would become one of the most famous biological control successes in forest entomology of all time (Embree 1966; Murdoch et al. 1985; Roland and Embree 1995; Kenis et al. 2017). Embree and his colleagues introduced several parasitoid species from Europe, two of which, the tachinid Cyzenis albicans and the ichneumonid Agrypon flaveolatum, began to cause high levels of mortality in winter moth populations after 4–5 years (Fig. 9.3a). By 1962, winter moth densities had declined to non-pest status, where they have remained ever since (Fig. 9.3a). Hassell (1980) presented a simulation model of C. albicans impact on winter moth that appears to explain why in Nova Scotia it was effective at suppressing winter moth populations, whereas it seemed to play a minor role in the population studied by Varley and Gradwell in England. The model was built on his earlier life table studies of C. albicans in England (Hassell 1968, 1969a, 1969b).
Similar biological control efforts were undertaken in the 1970s following an introduction of winter moth to Southwest British Columbia in Canada. Winter moth densities there soon declined following the onset of high levels of parasitism, mainly by the tachinid C. albicans (Roland 1986; Roland and Embree 1995). Yet another successful biological control effort was initiated by Elkinton et al. (2018, 2021) (Fig. 9.3b) against an outbreak of winter moth that appeared in the northeastern United States in the late 1990s (Fig. 9.1a) Elkinton et al. (2010). This effort was based solely on the release of the tachinid C. albicans, because Agrypon flaveolatum, the other parasitoid released in Canada, was deemed too much of a generalist and also of uncertain taxonomy. Over 14 years Elkinton and his colleagues established the fly at 41 release sites in New England and observed a substantial decline in winter moth densities (Fig. 9.3b) (Elkinton et al. 2018, 2021).
9.4.6 Population Ecology in North America
Roland (1990b) analyzed the decline of winter moth densities associated with the onset of parasitism by C. albicans in Nova Scotia and in British Columbia. He concluded that the decline was caused mainly by predation rather than parasitism and that the presence of C. albicans enhanced predation rates on winter moth pupae. He proposed several possible mechanisms for this phenomenon, which included reductions of winter moth densities to levels below which predators were saturated and caused inversely density-dependent mortality, or that parasitized pupae provided a food resource available in the spring months following the emergence of un-parasitized pupae in November and December. He further provided evidence that pupal predators caused density-dependent mortality that regulated the low-density populations of winter moth following the population decline induced by the presence of C. albicans (Roland 1994, 1995). Broadley et al. (2022) analyzed data from the recent biological control success in the northeast United States and confirmed Roland’s findings that low-density populations of winter moth following the onset of high parasitism by C. albicans were regulated by density-dependent predation by a suite of pupal predators. Broadley et al. (2019) also discovered a parasitoid, Pimpla aequalis that consisted of two cryptic species causing density-dependent mortality of winter moth pupae. Broadley et al. (2022) found no evidence in support of Roland’s findings that the presence of C. albicans enhanced predation on winter moth pupae.
Other research on winter moth population ecology in North America includes the life table studies of outbreak populations of winter moth in stands of red oak, Qurecus rubra, in Nova Scotia prior to the establishment of parasitoids (Embree 1965). Embree found that the main cause of population change in outbreak populations was synchrony of winter moth hatch with budburst, confirming similar conclusions reached by Varley et al. (1973) in England. In years where spring occurred phenologically early, hatch was well synchronized with budburst, yielding high larval survival. In contrast, in years where springtime warming came later, synchrony was poor and larval survival low. Embree’s research was followed up by MacPhee et al. (1988), who studied the lower-density populations of winter moth that existed on apple trees in Nova Scotia over the decade that followed the population decline induced by C. albicans in the early 1960s. He found that both C. albicans and A. flaveolatum caused parasitism in the range of 10 to 20%, far lower than the values observed by Embree in high-density populations in the early 1960s. These findings reinforce the idea that C. albicans has its biggest impact on high-density populations of winter moth. A principal reason is that this species is attracted to defoliated trees and oviposits tiny (micro-type) eggs on partially eaten leaves (Hassell 1968, 1980; Roland 1990a; Roland et al. 1995). Winter moth becomes parasitized by C. albicans only when the larva consumes the egg. These eggs then hatch, and the larval fly migrates to the salivary glands of the winter moth larva, where it stays until the moth stops feeding and drops to the ground to pupate. After this, the larval fly completes development, kills the winter moth pupa and forms a puparium inside the pupal cadaver.
9.4.7 Recent European Studies
In recent years, European research has focused mainly on the outbreaks of winter moth in northern Fennoscandia (Tenow et al. 2007; Jepsen et al. 2008). Winter moth outbreaks occur approximately every 10 years in the mountain birch (Betula pubescens czereapanovii) forests of that region in synchrony with, but lagging 2–3 years behind, those of another well-studied geometrid, the autumnal moth, Epirrita autumnata (Tenow et al. 2007). Jepsen et al. (2008) showed that outbreak populations of winter moth in this region were moving to higher altitudes in response to climate change (Fig. 9.4a) and were moving into forests formerly occupied only by autumnal moth. Consecutive outbreaks of both species are threatening widespread mortality of the mountain birch forests. Vindstad et al. (2022) documented the more recent spread of winter moth into willow (Salix) stands in the subarctic tundra of northeastern Fennoscandia.
Jepsen et al. (2009a, 2009b) used multitemporal remotely-sensed data of leaf-out and defoliation to show that favorable synchrony of winter moth hatch with budbreak fueled the synchronous outbreak of winter moths during the increase phase of the population cycle. The spatial synchrony was reduced during the peak and declining phase of the outbreak. Analyses by Tenow et al. (2013) indicated that waves of defoliation by winter moth spread from east to west across Europe approximately every 10 years. However, subsequent analyses challenged that conclusion (Jepsen et al. 2016), and no underlying mechanism for such a phenomenon has been proposed, especially since weather systems at that latitude move from west to east and winter moth females are incapable of flight.
Vindstad et al. (2013) reported the complex of larval parasitoids attacking winter moth and autumnal moth in Norway and compared it to the complex from other sites in Western Europe. These parasitoids included a total of 18 species, including five ichneumonids, three braconids, nine tachinids and one eulophid. The majority of these species occur in winter moth in northern Fennoscandia, with the exception of the tachinids, such as C. albicans, which do not occur there, despite being very common elsewhere (Vindstad et al. 2013). Recent studies by Schott et al. (2010) of winter moth mortality caused by these other larval parasitoid species often showed levels of mortality exceeding 50% in northern Norway. However, they do not appear to be responsible for the decline of outbreak populations. In contrast, Klemola et al. (2010) concluded from manipulative experiments that larval parasitoids are responsible for the decline of outbreak populations of the autumnal moth in northern Finland. Meanwhile, Schott et al. (2013) reported that outbreaks of winter moth in northern Norway are not caused by the release of winter moth populations from regulation at low density by invertebrate predation. It is evident that, despite all this research, the role of natural enemies in the dynamics of winter moth in northern Fennoscandia remains unresolved.
Other recent research has used modern molecular techniques to analyze the expansion of the winter moth’s range across Europe and the European origins of winter moth in North America. Gwiazdowski et al. (2013) sequenced the CO1 barcoding gene in a world-wide study of winter moth males collected using pheromone traps and found that nearly all the sampled individuals in the four North American populations shared a single haplotype. However, this haplotype was also found in winter moths collected from 10 of the 11 sampled European countries. This study was thus unable to determine the European origins of winter moth in North America. The lack of genetic diversity revealed by Gwiazdowski et al. (2013) was surprising given the fact that female winter moths are flightless, and thus strong biogeographic patterns might be expected. In a follow-up study, Andersen et al. (2017) examined gene regions called “microsatellites” that have greater sensitivity than the CO1 barcode gene for examining the genetic structure of populations. They showed that one possible explanation for the lack of genetic diversity in Europe found by Gwiazdowski et al. (2013) is that winter moth populations in central and western Europe (Fig. 9.5) represent a blend of populations from eastern Europe and the Iberian peninsula. They argue that this pattern arose as a result of widely separated forest refugia on the Iberian peninsula and in southeastern Europe during the last glacial maximum (Fig. 9.5).
Subsequent analyses of moths collected in the Mediterranean region have identified two additional glacial refugia: one in southern Italy and another in North Africa (Andersen et al. 2019b). A follow-up analysis showed that winter moth invaded northern Scandinavia via the United Kingdom instead of alternate routes via Denmark or eastern Europe (Andersen et al. 2021b). More recently, these microsatellite markers have been used to reexamine the geographic origins of the invasive winter moth populations in North America (Andersen et al. 2021a). These analyses show that each one of the four North American populations of winter moth (Nova Scotia, New England, British Columbia and Oregon) are all quite distinct from one another and probably represent separate introductions (Andersen et al. 2021a). In addition, the populations from Nova Scotia, British Columbia, and New England all appear to be introduced from western Europe (likely France or Germany), while the population in Oregon appears to be introduced from somewhere in the British Isles.
Other European studies have focused on the effects of climate change on the timing of winter moth hatch in spring. Winter moth larvae have been hatching earlier and earlier as spring temperatures have become warmer over the last several decades. Although winter moth is rarely a significant defoliator in central Europe, it is an important source of food for nesting birds in the spring. Migratory birds have timed their arrival based on solar cues and in recent years have arrived too late after winter moth larvae have finished feeding and dropped to the forest floor to pupate (Visser et al. 1998). Visser and Holleman (2001) showed that warmer springs have caused winter moths to desynchronize with budbreak of oaks (Quercus spp.), their principal host tree, and shift to other tree species that break bud earlier. They also showed that egg hatch in spring is influenced by factors more complex than predicted by growing-degree-day models that are widely used to predict hatch of most insects in the spring. Hatch times in their model were also influenced by the number of winter days below freezing. Hibbard and Elkinton (2015) applied this model with some success to egg hatch data in North America. Salis et al. (2016) proposed a revised model, wherein developmental rate of winter moth eggs as a function of temperature increased with egg age or egg development (see also Gray, 2018). Elkinton is currently attempting to fit versions of these models for egg hatch and bud-break to data from North America. Van Dis et al. (2021) have provided detailed information on the effects of temperature on embryonic development of winter moth eggs.
9.5 Case Study 2: Spongy Moth
9.5.1 Biology
Spongy moth, Lymantria dispar L. (formerly called gypsy moth) is another major defoliator, mainly of deciduous trees, that is native to both Europe and Asia. Three subspecies have been described (Pogue and Schaefer 2007): European spongy moth (Lymantria dispar dispar), Asian spongy moth (Lymantria dispar asiatica), and Japanese spongy moth (Lymantria dispar japonica). Although spongy moth females have wings and the Asian subspecies tend to be capable of flight, most populations of the European subspecies L. dispar dispar do not fly (Keena et al. 2008). Spongy moth females mate in mid-summer and lay egg masses that contain from 100‒1000 eggs on the stems of trees, rocks or other objects and cover them with their tawny brown body hairs. Larvae hatch in spring coincident with host tree budburst and develop through five (males) or six (females) larval instars until late June or early July, depending on latitude. Late-instar larvae in low-density populations seek daytime resting locations under bark flaps or on the forest floor, presumably as a defense against day active predators and parasitoids (Lance et al. 1987). Pupation typically occurs in these resting locations. Adults emerge in mid-summer. There is one generation per year.
9.5.2 Introduction to North America
European spongy moths (L. dispar dispar) were introduced into North America in 1868 or 1869 by Leopold Trouvelot for the purpose of various experiments. The insect escaped from his home in a suburb of Boston, Massachusetts and began to spread across the landscape. Trouvelot tried to notify local officials of the potential problem resulting from his accident, but his efforts were ignored until widespread defoliation in his neighborhood became apparent in the late 1880s. The Massachusetts state legislature allocated funds to eradicate spongy moth by mechanical removal of egg masses and applications of primitive pesticides such as lead arsenate (Spear 2005). This effort failed and spongy moth continued to spread, albeit quite slowly, since the females of the European strain of the species do not fly. Indeed, 140 years later, spongy moths are still spreading south and west in North America as shown in Fig. 9.2a and only occupy about 1/3 of their potential range (Figs. 9.6 and 9.7).
9.5.3 Host Preferences
Like winter moths, spongy moths feed on a wide range of host tree species, but perform best on oaks (Quercus spp), aspen (Populus), and birches (Betula) (Liebhold et al. 1995; Davidson et al. 1999). They will feed on many conifers and indeed on most tree species, especially if preferred hosts are unavailable or already defoliated. A handful of species are avoided altogether, even in stands that are otherwise completely defoliated. These species include ash (Fraxinus spp), silver maple (Acer saccharinum) and tulip poplar (Liriodendron tulipifera).
9.5.4 Impact on Forests and Trees
Defoliation is more frequent in forest stands that are dominated by tree species preferred by spongy moths, as described above, than in stands dominated by other tree species. In eastern North America, oaks (Quercus) dominate the forests in southern New England, the mid-Atlantic states and the Midwest. Aspen (Populus) dominated forests are often defoliated in the region around the Great Lakes (Fig. 9.6). These forests are most frequently defoliated by spongy moth and experience the greatest tree mortality (Campbell and Sloan 1977; Davidson et al. 1999).
Most hardwood trees defoliated > 50% by spongy moths will re-foliate in midsummer. However, those that fail to re-foliate at that time, or fail to re-foliate the following spring, will be killed, due to insufficient carbohydrate reserves (Kulman 1971). Defoliated trees become susceptible to attack by secondary organisms, such as the two lined chestnut borer, Agrilus bilineatus, or the shoestring fungus, Armillaria spp., and these agents are often the main causes of tree death (Campbell and Sloan 1977; Wargo 1977). Repeated defoliations in consecutive years can lead to levels of tree mortality exceeding 50% (Kegg 1973; Campbell and Sloan 1977). Other studies show less mortality following defoliation (Brown et al. 1979; Gansner et al. 1993). Campbell and Sloan (1977) analyzed the impact of spongy moth on stands from 1911 to 1931 in New England and reported that defoliation occurred most frequently on oak-dominated stands and that oaks were the most likely to die. Dominant trees survived better than ones that were subdominant or suppressed. Non-favored host trees, such as white pine and red maple, were more likely to die after one defoliation than oak trees. Morin and Liebhold (2016) analyzed the impact of spongy moth defoliation on changes in the tree species composition data collected by the USDA Forest Service between 1975 and 2010. They found that most of the stands with repeated defoliation in the northeastern USA were oak-dominated, and the effect of defoliation was to hasten the process of replacement of overstory oaks with other species such as maple (Acer), which are less preferred by spongy moth. Even though the volume or basal area of oak was increasing across this region due to tree growth, mortality of the younger age classes of oaks contributed to the overall decline of oaks and replacement by other species.
9.5.5 Spread of Spongy Moth
The enormous spatial detail evident in the spongy moth pheromone trap catch data (Fig. 9.2a) across the landscape, and the long time period over which spread has been monitored, have allowed investigators to study the rate of spread of spongy moths and make important contributions to the theory of spread of invasive organisms. Liebhold et al. (1992) compared historical rates of spongy moth spread (1900–1989) with predictions made using the spread model of Skellam (1951). The Skellam model consists of two components: exponential population growth defined by the parameter ‘r’ and diffusion analogous to molecular diffusion defined by the parameter D. The model predicts that the rate of spread V of an invasion front is constant: V = 2√rD. Liebhold et al. (1992) estimated both parameters from earlier studies of spongy moth population growth and diffusion based on dispersal of first-instar larvae that spin down on threads from tree canopies and are blown in the wind. Experimental studies of that process (Mason and McManus 1981) suggest that most such larvae spread only a few hundred meters, but a few of them spread several kilometers. The Skellam model based on these parameters predicted that spongy moth dispersal would be about 2 km/year. The spongy moth spread prior to 1966 varied between 2 and 10 km/year compared to 20.78 km/year after 1996. Liebhold et al. (1992) concluded that the discrepancy between predicted and observed spread was due to accidental human movement of spongy moth life stages which form isolated populations ahead of the advancing population front and thereby accelerate spread.
Analyses of spongy moth spread were greatly enhanced by implementation of regional grids of pheromone traps (Fig. 9.2a, 9.8a). Analyses of such data from the central Appalachians (Sharov et al. 1995, 1996, 1997) indicated a rate of spread that varied yearly and ranged from 17 to 30 km/year. These data show that clumps of small populations of spongy moths arise many kilometers in front of the infested zone (Figs. 9.2a, 9.8a), and their growth and coalescence contribute significantly to the rate of spread. These data suggest that spread of spongy moth is an excellent example of stratified dispersal (Hengeveld 1989), consisting of a short-range process governed by larval dispersal and a longer-range process governed by human transport of spongy moth egg masses. The latter process has long been understood to be a central feature of the spongy moth system. Spongy moths lay the overwintering egg masses in midsummer on backyard objects, such as lawn furniture, that are readily transported in succeeding months elsewhere in the United States. As a result, new infestations arise many kilometers from the generally infested area or indeed anywhere else in North America. Models of stratified dispersal (Shigesada and Kawasaki 1997) were fit to the spongy moth system (Sharov and Liebhold 1998a). These analyses form the theoretical basis of the spongy moth Slow the Spread Program (Sharov et al. 1997, 1998, 2002a; Sharov and Liebhold 1998a, 1998b; Tobin and Blackburn 2007) discussed below. Suppression of these incipient populations, arising ahead of the invasion front, slows the spread.
Understanding the survival and expansion of incipient populations thus became a key feature of managing spongy moth. Such populations are governed by Allee effects (Fig. 9.8b), which express the survival or growth of populations as a function of population densities. At the very low densities characteristic of newly founded populations, survival or population growth of many species increases with population density. At higher densities, in virtually all populations survival or growth rates decline to an equilibrium that represents either the carrying capacity, or else a lower-density equilibrium maintained by natural enemies. Allee effects refer to the positive density dependence at lower densities, and they can be weak or strong (Taylor and Hastings 2005). If they are strong, then at very low densities there exists what is called the Allee threshold (Fig. 9.8b). At densities above the threshold, populations steadily increase. When populations are below the threshold, however, densities typically decline to extinction. In other words, the low-density Allee threshold is an unstable equilibrium. There are several possible causes of low-density Allee effects in spongy moth populations, including predation (see below), but probably the most common cause at the very lowest densities characteristic of incipient populations is failure to locate mates. The implication of this is that many incipient populations of spongy moth will decline to extinction on their own accord. Indeed, data suggest that this frequently occurs (Liebhold et al. 2016). Eradication of such populations with pesticides or indeed mating disruption (Sharov et al. 2002b) is entirely feasible because even if the treatment fails to kill all the spongy moths it will surely vastly lower their densities and thus hasten their natural tendency to decline to extinction.
Subsequent analyses of spongy moth spread have shown that the rate of spongy moth spread declines with the strength of Allee effects (Tobin et al. 2007, 2009), which varies in time and space across the landscape. The strength is measured by the intercept of the plot shown in Fig. 9.8b with the vertical axis; it is strongest when the intercept with the vertical axis (below the figure) is most negative. For example, Tobin (2007) reported that there were strong Allee effects and, as a result, slower spread in parts of the Midwest compared to Great Lakes or Appalachian regions.
An exciting recent finding (Tobin et al. 2014) is that spongy moth populations in North Carolina have stopped spreading, and indeed have retreated northward in recent years. Tobin et al. (2014) suggest that in that region spongy moths have exceeded temperature maximums that inhibit optimal growth and further spread to southern states, and the northward retreat may be due to climate change. These findings imply that spongy moths may never occupy southern regions of the Midwest with highly susceptible oak forests (Fig. 9.6).
9.5.6 History of Spongy Moth Control
Efforts to control spongy moth in Massachusetts began in 1890, with a large program funded by the state legislature. The program focused on an attempt to mechanically destroy spongy moth egg masses, which are present on the trunks of trees from August through April each year. In addition, there was a large effort to spray the larvae with pesticides, mainly with lead and copper arsenate. There was little or no appreciation in those days of the environmental danger posed by these toxins. Furthermore, they were largely ineffective and failed to stem the spread of the population.
In 1905, the US Department of Agriculture launched what became the most extensive worldwide effort for biological control of an invasive forest insect ever conducted. Twelve species of parasitoids became established of the 34 species that were released over several decades. Fuester et al. (2014) provide the most recent of several reviews of this effort. These included the egg parasitoid Ooencyrtus kuvanae (Howard) [Hymenoptera Encyrtidae]; three tachinid [Diptera] species: Compsilura concinnata (Meigen), Parasetigena silvestris (Robineau-Desvoidy), and Blepharipa pratensis (Meigen); a braconid Cotesia melanoscelus (Ratzeburg) and an ichneumonid Phobocampe disparis (Viereck) which attack the larval stage of spongy moth. Pupal parasitoids established were two hymenopterans: the chalcid Brachymeria intermedia (Ness) (Chalcidae) and the ichneumonid Pimpla disparis (Viereck). Of these, O. kuvanae and P. disparis were introduced from Japan, the other species from Europe. Compsilura concinnata was introduced to North America in 1906 and has gained some notoriety because Boettner et al. (2000) showed that it has become the dominant source of mortality on several native species of giant silk moths (Saturniidae) and is probably responsible for the decline of these species since the nineteenth century. On the other hand, Elkinton et al. (2006) showed that the same parasitoid was probably responsible for the extirpation of the invasive brown tail moth, Euproctis chrysorrhea, over much of its invasive range in the northeastern United States.
Unfortunately, these parasitoids did not prevent spongy moth outbreaks. Williams et al. (1992) published the only long-term data on parasitism by these species and concluded that none of them regulated spongy moth density. The results of this study confirmed the conclusions drawn by earlier investigators: that parasitoids played a limited or equivocal role in the population dynamics of spongy moth in North America (Campbell 1975; Reardon 1976; Elkinton and Liebhold 1990). In addition to parasitoids, biological control introductions included predatory beetles, such as Calosoma sychophanta (Weseloh 1985) and pathogens such as Entomophaga maimaiga from Japan (Fuester et al. 2014). That pathogen was initially collected and released in 1910 and 1911 in the Boston area but was not established (Speare and Colley 1912). The recent invasion of spongy moth populations by E. maimaiga in North America that began in 1989 (see below) was evidently an accidental or inadvertent introduction (Hajek 2007). Entomophaga maimaiga was recently established in Bulgaria from where it has spread to other European countries and has become quite common (Hajek et al. 2020). But with the notable possible exception of E. maimaiga after 1989, none of these introductions prevented spongy moth outbreaks.
Following World War II, the pesticide DDT became widely available. It was cheaper and more effective than any previous pesticide. In the succeeding decades, widespread aerial application of DDT was made against spongy moth. Applying pesticide by air allowed application at a landscape level, something that was never feasible or affordable from the ground. Entomologists in those days were convinced that DDT was a new tool that would solve most insect problems. By the 1960s, however, the environmental costs of DDT and related compounds were evident and were popularized by the famous book Silent Spring by Rachel Carson. DDT and its breakdown products persist indefinitely in the environment and accumulate in the fatty tissue of many animals. It was particularly damaging to birds, especially those at the end of long food chains, such as eagles and ospreys. DDT and other chlorinated hydrocarbon insecticides were banned in the late 1960s and 1970s. The Environmental Protection Agency was established, and laws were passed to require safety testing of all pesticides. Nevertheless, populations of birds such as eagles and ospreys took many decades to recover, a process that goes on to this day.
Meanwhile, new pesticides were developed and used against spongy moth. In the early 1980s aerial applications of carbaryl were very popular. Carbaryl gave way to diflubenzuron, an insect growth regulator. By the end of the decade the bacterial insecticide Bacillus thuringiensis (Bt.) became popular. Its advantage was that it affected only foliage-eating insects, and not the adult stages of their insect natural enemies. Other bacterial insecticides such as spinosad were added to the mix in subsequent decades. Thus, in the modern era, we now have much safer pesticides that affect a more narrow spectrum of target and nontarget insects. In the northeastern states large scale aerial application of pesticides largely ceased after 1990 (Fig. 9.9b), coincident with the arrival of a new fungal pathogen of spongy moth, E. maimaiga (see below). It appears likely that the days of aerial application of any pesticides against spongy moth in New England are finished. We now know that the spongy moth outbreaks will subside on their own, and the forests will recover, even if there is significant tree mortality. Even the modern pesticides with a narrow spectrum will kill many nontarget insects and aerial applications are too expensive to justify for the governmental agencies charged with carrying them out. Applications to individual shade trees, however, are another matter. Homeowners place high value on these trees which provide beauty and shade to their yards. If a shade tree dies, it is expensive to remove. Homeowners are thus willing to spend significant funds to protect their trees, and many tree care professionals are available to help them to do that. The small scale of such applications presumably has a limited impact on non-target species at the landscape scale.
The federal effort against spongy moth in recent years has focused on the “Slow the Spread” project (Tobin and Blackburn 2007) (Fig. 9.2a). This involves annually deploying 80,000 to 100,000 traps baited with spongy moth pheromone each year in a grid along a front that extends from Minnesota to North Carolina. The objective of this effort is to identify incipient populations arising ahead of the invasion front that facilitate spread, as described above. Efforts are thus made to suppress them and slow the overall rate of spread of spongy moth. While this effort is expensive, cost–benefit analyses have shown that it is justified (Sharov and Liebhold 1998c). To suppress isolated populations, the program mostly relies on aerial applications of pheromones in small slow-release dispensers such that spongy moth males in treated areas are unable to locate females. Consequently, many females go unmated (Sharov et al. 2002b). This approach is called mating-disruption or the confusion technique (Carde and Minks 1995). It has been widely applied against agricultural pests such as pink bollworm, Pectinophora gossypiella, on cotton, but this is one of the only applications that has been widely applied against a forest insect. Another more widely used eradication technique involves application of microbial pesticides such as Bacillus thuringiensis (Bt) (Hajek and Tobin 2010).
A parallel effort is used to detect and eradicate isolated populations of spongy moth that arise far from the invasion front in the western and southern United States, where spongy moth egg masses are transported inadvertently by homeowners arriving from the infested region in the east. Again, the strategy is to annually deploy networks of thousands of traps that are used to detect newly-founded populations. Following detection, these populations are eradicated, mostly using aerial applications of the microbial pesticide Bacillus thuringiensis. Of particular concern are populations of Asian spongy moths arriving on ships from East Asia, where the flying female spongy moths are attracted to lights associated with various ports in Asia and thus often deposit egg masses in large numbers on ships in the ports. Asian spongy moths represent a major threat to North America, because, once established, they can spread across the continent very rapidly, and they attack different tree species, including conifers (Baranchikov and Sukachev 1989). Thus, a major effort has been made to locate spongy moth egg masses on cargo and ships arriving from East Asian ports and prohibit imports of contaminated cargo. Recent theoretical studies show that eradication of incipient populations is far more feasible than originally thought (Liebhold et al. 2016).
9.5.7 Population Ecology of Spongy Moth
Robert Campbell, of the US Forest Service, in the 1960s and 1970s, led the first comprehensive research aimed at understanding the population ecology of spongy moth in North America. Campbell and Sloan (1978a) suggested that predation by small mammals, in particular the white-footed mouse, Peromyscus leucopis, feeding on the late larval and pupal stages, was the key to maintaining populations at low density in the years between outbreaks. Predation by birds, in contrast, was much less important. Many bird species feed to some extent on spongy moth caterpillars, but many are also deterred by the hairs on the integument.
Elkinton et al. (1996) presented results of research initiated in the 1980s at two sites in Massachusetts that confirmed the importance of small mammal predation on low-density spongy moth populations. They showed that spongy moth populations would rise when populations of white-footed mice declined. Furthermore, they showed that mouse populations fluctuate with the acorn crops, their major overwintering food source. As is true with many tree species, acorn crops vary enormously from year to year. A variety of weather conditions, such as a late spring frost or mid-summer drought, can nearly eliminate the acorn crop. They also showed that when acorn crops failed, as in the autumn of 1992 (Fig. 9.10), mouse populations had declined dramatically by the following summer, and spongy moth populations therefore increased (Fig. 9.10). All of this occurred at low spongy moth density, when they were in a non-outbreak phase (egg mass densities < 100/ha).
Somewhere above one hundred egg masses per acre, a density threshold is reached, beyond which predation by mice or other small mammals, such as shrews, declines with increasing spongy moth density. Unlike spongy moth parasitoids, changes in the density of vertebrate predators such as mice or birds are fairly constrained. Birds defend territories and so do mice. Thus, the population densities of mice rarely increase beyond about 100 mice per ha. Spongy moths, in contrast, can increase from 1 to 100 to 10,000 egg masses per ha, which is characteristic of outbreak populations. At these higher densities, mice or birds can feed all day on spongy moth and never make a dent in the population, whereas, at lower spongy moth densities, the mice may consume most of the spongy moth pupae in the forest. Therefore, as spongy moth density increases, there is decline in the percent mortality caused by mice and other generalist predators. Thus, vertebrate predators play almost no role in regulating outbreak populations. With many caterpillar species, parasitoids can regulate density and prevent outbreaks because their numbers can increase along with their hosts. Unfortunately, introduced and native parasitoids that attack spongy moth in North America do not do this effectively. Their numbers are constrained for reasons that are poorly understood, and they never cause very high levels of parasitism. So, once spongy moth densities reach a threshold in the vicinity of 100 egg masses per acre, the spongy moth population will grow inexorably over the next one or two years into an outbreak phase that results in widespread defoliation.
Outbreak populations become limited only by the availability of green foliage. Few spongy moth larvae actually starve in outbreak populations, but many fail to get sufficient food resources. As a consequence, the adults that arise from such populations are smaller and the females might lay 100 eggs per mass, instead of 600 (Campbell and Sloan 1978a). More importantly, there is a virus disease called nuclear polyhedrosis virus (LdNPV) that causes epidemics in these outbreak populations and may kill 99% of larvae before they reach the pupal stage (Campbell and Podgwaite 1971). Such viruses are common in outbreak populations of many insect species. Virus diseases reach epidemic proportions in outbreak populations because high caterpillar densities increase disease transmission. When the caterpillar dies from LdNPV, the virus causes the caterpillar cadaver to liquefy and spread virus particles over the leaf surface. Transmission occurs when a healthy caterpillar consumes virus particles released by these liquefied cadavers. Mortality from LdNPV starts in the early larval stages but grows exponentially in the late larval stage and peaks just before the caterpillars form pupae (Campbell and Podgwaite 1971; Murray et al. 1989). It is this epidemic that brings an end to spongy moth outbreaks and causes the populations to retreat back to low density. Therefore, outbreaks will typically last for 1 to 3 years before this population collapse happens. In the years following collapse of the outbreak, predation by small mammals resumes as the dominant force of mortality that maintains spongy moth at low density (Campbell and Sloan 1978b).
Campbell and Sloan (1978b) believed that spongy moth was a multi-equilibrium system (see Chapter 5) with a low-density equilibrium maintained by predators, mainly mice, and a high-density equilibrium wherein foliage supply and the resulting decline in fecundity, coupled with epizootics of LdNPV, limited further expansion of spongy moth densities and ultimately caused the collapse of outbreak populations. While it is very clear that there is indeed an upper limit to spongy moth densities, and that LdNPV plays a major role in the collapse of outbreaks, evidence for the low-density equilibrium remains undemonstrated. Campbell believed that predation rates by small mammals increased with spongy moth density at the lowest spongy moth densities but lacked supporting evidence. Unlike parasitoids, densities of small mammal predators do not increase in response to increased spongy moth density. Mouse densities are governed in large part by acorn crops, their principal overwintering food source. In contrast, spongy moth pupae and late instar larvae represent an extremely ephemeral food resource for mice at a time of year when they have many other things to feed on. Predation rates, if they are to increase with spongy moth density, must, in response, entail a change in foraging behavior of the predator (a Type III functional response) (Holling 1959) to increasing density of prey. In field experiments, Elkinton et al. (2004) showed that mice exhibited a Type II functional response, wherein rates of predation decline steadily as densities increase from the lowest spongy moth densities. This implies that mice cannot serve to regulate spongy moth populations at low density. This type of predation may contribute to the Allee effect in low-density spongy moth populations, as discussed above.
Dwyer et al. (2004) developed a model of spongy moth populations that combined the effects of LdNPV and small mammal predators. The model predicted regular outbreaks of spongy moths with an approximate 10-year periodicity. Fundamentally, this was a pathogen-driven model analogous to earlier models (e.g. Anderson and May 1981), but the addition of predators added an unstable low-density equilibrium to the system. Even a minor amount of stochasticity, however, resulted in quasi-periodic oscillations (Fig. 9.11B) that matched those of spongy moth defoliation data in New Hampshire (Fig. 9.11A) characterized by chaotic dynamics (May 1975) that make them susceptible to dynamical change with small environmental perturbations or small changes in model parameter values (Fig. 9.11C). Subsequent analyses of spongy moth defoliation data confirmed the existence of such periodicities in the spongy moth system (Bjørnstad 2000).
The Dwyer et al. (2004) model was elaborated by Bjørnstad et al. (2010) and applied to defoliation data. The revised model replaced the Type III functional response of predation with a Type II functional response, which made a low-density equilibrium caused by predators impossible. Indeed, there exists no evidence to support such an equilibrium. These analyses suggested the existence of a dominant 10-year cycle with a subdominant four-year cycle (Johnson et al. 2006a; Haynes et al. 2009a). Allstadt et al. (2013) analyzed 86 years of defoliation data, the longest available for/in North America, and concluded that population cycles appeared or disappeared four times over the duration of the spongy moth infestation in North America (Fig. 9.12B).
Another conspicuous feature of the spongy moth population system is that populations fluctuate in synchrony with one another across the landscape (Williams and Liebhold 1995a, 1995b; Peltonen et al. 2002; Liebhold et al. 2004; Johnson et al. 2006a, 2006b; Bjørnstad et al. 2008; Haynes et al. 2013; Allstadt et al. 2015). This phenomenon is nearly ubiquitous with most forest insects (Liebhold and Kamata 2000). Dispersal from one population to another can synchronize adjacent populations, but for spongy moth, and most other forest insects, this occurs over far too short a distance to account for the regional synchronies observed (Peltonen et al. 2002). Instead, the standard explanation for this phenomenon involves the Moran (1953) effect. Moran was a statistician who studied the famous snowshoe hare-lynx predator prey oscillation in Canada. He showed that model time series of such populations in different locations would come into synchrony with one another, provided they were influenced by a common random factor, such as synchronous weather. The shared weather conditions are not responsible for the oscillation, but they do explain why snowshoe hares or forest insects typically oscillate in synchrony with one another across much of northern Canada. The synchrony breaks down at greater distances because weather conditions become uncorrelated at these distances. Bjørnstad et al. (1999) developed statistical methods to detect such synchrony and how it declines with distance between two or more populations (see Fig. 9.4b, c). Moran’s model assumed that the dynamics of spatially separated populations were all governed by the same density-dependent processes. In fact, these dynamics undoubtedly vary somewhat in space. Peltonen et al. (2002) showed that populations with similar but distinct dynamical parameters still exhibited spatial synchrony, as Moran described, but the synchrony declined with distance more sharply than the synchronizing weather conditions. Haynes et al. (2009b) utilized the model of Bjørnstad et al. (2010) and analyzed data on the spatial synchrony of spongy moths, white-footed mice, and acorn crops in the northeastern United States. All three are synchronized out to a distance of approximately 1000 km. They concluded that synchrony of acorn crops was the main cause of spongy moth and mouse synchrony, as opposed to the independent regional stochasticity (i.e. weather conditions) directly affecting each of the latter two species. The synchrony of all three is evident on a small spatial scale (ca 10 km) in Fig. 9.10.
In 1989, a dramatic change occurred to spongy moth populations with the accidental introduction of a fungal pathogen of spongy moth, Entomophaga maimaiga, from Japan (Andreadis and Weseloh 1990; Hajek et al. 1990b). That year, the fungus caused extensive mortality in both high and low-density populations throughout southern New England. The following year, the infection spread over the rest of New England and halfway across Pennsylvania (Elkinton et al. 1991). The rapid spread was due to the fact that spongy moth cadavers killed by the fungus produce conidia that are blown in the wind across the landscape. Subsequent research showed the fungus depends on rainy conditions in May and June for successful transmission to healthy larvae, and, indeed, 1989 was an especially rainy year. Beginning in 1991, spongy moth researchers worked to spread E. maimaiga to Michigan (Smitley et al. 1995) and to Virginia (Hajek et al. 1996), but the fungus spread rapidly on its own, so that by about 1996 all of the areas infested by spongy moth in the northeastern United States were infested with the fungus (Hajek 1997, 1999). The fungus caused a major change in status of spongy moth as a serious forest pest in New England states. Spongy moth populations in that region declined to low density where they have mostly remained for the last 35 years (Fig. 9.13). In contrast, spongy moth populations in areas further south, such as Pennsylvania, have continued to have periodic outbreaks despite the presence of the fungus (Morin and Liebhold 2016). Laboratory tests demonstrated that the fungus does best in cooler conditions (Hajek et al. 1990a). Temperatures in May and June in the mid-Atlantic states are much warmer than in New England.
Studies of the interaction of spongy moth fungal and viral pathogens demonstrated that E. maimaiga develops more quickly and outcompetes LdNPV when both pathogens affect the same larva (Malakar 1997; Malakar et al. 1999). The same is true for infections of E. maimaiga and parasitoid larvae in spongy moth larvae. Hajek et al. (2015) (Fig. 9.14a) demonstrated that E. maimaiga has now become the dominant mortality factor in both low and high-density populations of spongy moth. However, Liebhold et al. (2013) demonstrated that LdNPV still causes comparable levels of density-dependent mortality in outbreak populations in the presence of E. maimaiga as it had before the fungal pathogen was introduced in 1989 (Fig. 9.14b). Various studies indicate that rainfall in May and June are critical to transmission of E. maimaiga (Hajek et al. 1990a; Hajek 1999; Reilly et al. 2014). A recent outbreak of spongy moth in New England (Fig. 9.1b; Pasquarella et al. 2018), the first widespread one since 1981, was likely caused or facilitated by three consecutive years of drought conditions in May and June beginning in 2014. Thus, rainfall has likely become a critical feature in promoting or suppressing spongy moth outbreaks. Most of the time series analyses of spongy moth defoliation data described above were applied to data collected prior to widespread establishment of E. maimaiga, so perhaps it is still too early to tell how it will affect the overall dynamics of spongy moth. For example, the disappearance of the population cycles after 1996 described by Allstadt et al. (2013) might be due to this major new source of mortality. Unlike the viral pathogen LdNPV, which only causes major epizootics in outbreak populations of spongy moth, E. maimaiga causes high levels of mortality in both low- and high-density populations (Hajek 1999; Fig. 9.14c). As such, it may play a significant role in preventing the onset of outbreaks in contrast to LdNPV. Even so, E. maimaiga is weakly density dependent because transmission depends on conidia that spread from nearby high-density populations (Bittner et al. 2017; Elkinton et al. 2019). Thus, E. maimaiga might contribute to the development of a low-density equilibrium, whose existence has not yet been demonstrated in spongy moth populations. Kyle et al. (2020) developed a population model of the impact of E. maimaiga on spongy moth population dynamics. Recent analyses by Liebhold et al. (2022) demonstrate that E. maimaiga has reduced the intensity of spongy moth outbreaks but not necessarily their frequency. Further studies and longer population time series are needed to resolve its role in low-density population dynamics of spongy moth.
As described above, spongy moth has been exhaustively researched both from a population dynamic and from a management perspective. The extensive data on spongy moth defoliation and pheromone trap catch is almost certainly the most extensive such data for any species and has allowed researchers to make significant contributions to the general theory of population spread and eradication of invasive species. Analysis of spongy moth population data has made important contributions to the general theory of population cycles, Allee effects, and spatial synchrony of population fluctuations.
In Table 9.1, we list what we believe are the most important or damaging foliage-feeding forest insects in the world. We list the geographical range, the host tree species, and key references that give readers access to the literature on these species. We do not include the two species we have already discussed at length: winter moth, Operophtera brumata and spongy moth, Lymantria dispar.
References
Alfaro RI, Maclauchlan LE (1992) A method to calculate the losses caused by western spruce budworm in uneven-aged Douglas-fir forests of British-Columbia. Forest Ecol Manag 55(1–4):295–313. https://doi.org/10.1016/0378-1127(92)90107-K
Alfaro RI, Taylor SP, Wegwitz E et al (1987) Douglas-fir tussock moth damage in British Columbia. Forest Chron 63(5):351–355. https://doi.org/10.5558/tfc63351-5
Alfaro RI, Taylor S, Brown G et al (1999) Tree mortality caused by the western hemlock looper in landscapes of central British Columbia. Forest Ecol Manag 124(2–3):285–291. https://doi.org/10.1016/S0378-1127(99)00073-0
Alfaro RI, Berg J, Axelson J (2014) Periodicity of western spruce budworm in Southern British Columbia, Canada. Forest Ecol Manag 315:72–79. https://doi.org/10.1016/j.foreco.2013.12.026
Allen DC (1972) Insect parasites of the saddled prominent, Heterocampa guttivitta (Lepidoptera: Notodontidae), in the northeastern United States. Can Entomol 104(10):1609–2162. https://doi.org/10.4039/Ent1041609-10
Allen DC (1973) Fecundity of the saddled prominent. Heterocampa guttivitta. Ann Entomol Soc Am 66(6):1181‒1183.https://doi.org/10.1093/aesa/66.6.1181
Allstadt AJ, Haynes KJ, Liebhold AM et al (2013) Long-term shifts in the cyclicity of outbreaks of a forest-defoliating insect. Oecologia 172:141–151. https://doi.org/10.1007/s00442-012-2474-x
Allstadt AJ, Liebhold AM, Johnson DM et al (2015) Temporal variation in the synchrony of weather and its consequences for spatiotemporal population dynamics. Ecology 96(11):2935–2946. https://doi.org/10.1890/14-1497.1
Ammunét T, Heisswolf A, Klemola N et al (2010) Expansion of the winter moth outbreak range: no restrictive effects of competition with the resident autumnal moth. Ecol Entomol 35(1):45–52. https://doi.org/10.1111/j.1365-2311.2009.01154.x
Andersen JC, Havill NP, Caccone A et al (2017) Postglacial recolonization shaped the genetic diversity of the winter moth (Operophtera brumata) in Europe. Ecol Evol 7(10):3312–3323. https://doi.org/10.1002/ece3.2860
Andersen JC, Havill NP, Broadley HJ et al (2019a) Widespread hybridization among native and invasive species of Operophtera moths (Lepidoptera: Geometridae) in Europe and North America. Biol Ivasions 21:3383–3394. https://doi.org/10.1007/s10530-019-02054-1
Andersen JC, Havill NP, Mannai Y et al (2019b) Identification of winter moth (Operophtera brumata) refugia in North Africa and the Italian Peninsula during the last glacial maximum. Ecol Evol 9(24):13931–13941. https://doi.org/10.1002/ece3.5830
Andersen JC, Havill NP, Caccone A et al (2021a) Four times out of Europe: Serial invasions of the winter moth, Operophtera brumata, to North America. Mol Ecol 30(14):3439–3452. https://doi.org/10.1111/mec.15983
Andersen JC, Havill NP, Griffin BP et al (2021b). Northern Fennoscandia via the British Isles: evidence for a novel post-glacial recolonization route by winter moth (Operophtera brumata). Frontiers of Biogeography 13(1):e49581. https://doi.org/10.21425/F5FBG49581
Andersen JC, Havill NP, Boettner GH et al (2022) Real-time geographic settling of a hybrid zone between the invasive winter moth (Operophtera brumata L.) and the native Bruce spanworm (O. bruceata Hulst). Mol Ecol. https://doi.org/10.1111/mec.16349
Anderson JF, Kaya HK (1976) Parasitoids and Diseases of the Elm Spanworm. J New York Entomol S 84(3):169–177. https://www.jstor.org/stable/25009007. Accessed 18 October 2022
Anderson L, Carlson CE, Wakimoto RH (1987) Forest fire frequency and western spruce budworm outbreaks in western Montana. Forest Ecol Manag 22:251–260. https://doi.org/10.1016/0378-1127(87)90109-5
Anderson RM, May RM (1981) The population dynamics of microparasites and their invertebrate hosts. Philos T Roy Soc B 291(1054):451–524. https://doi.org/10.1098/rstb.1981.0005
Andreadis TG, Weseloh RM (1990) Discovery of Entomophaga maimaiga in North American gypsy moth, Lymantria dispar. P Natl Acad Sci USA 87(7):2461–2465. https://doi.org/10.1073/pnas.87.7.2461
Appleby JE, Bristol P, Eickhorst WE (1975) Control of fall cankerworm. J Econ Entomol 68(2):233–234. https://doi.org/10.1093/jee/68.2.233
Arnaldo PS, Chacim S, Lopes D (2010) Effects of defoliation by the pine processionary moth Thaumetopoea pityocampa on biomass growth of young stands of Pinus pinaster in northern Portugal. Iforest 3(6):159–162. https://doi.org/10.3832/ifor0553-003
Asaro C, Allen DC (2001) History of a pine false webworm (Hymenoptera: Pamphiliidae) outbreak in northern New York. Can J Forest Res 31:181–185. https://doi.org/10.1139/x00-147
Austarå Ø, Orlund A, Svendsrud A et al (1987) Growth loss and economic consequences following two years defoliation of Pinus sylvestris by the pine sawfly Neodiprion sertifer in West-Norway. Scand J Forest Res 2(1–4):111–119. https://doi.org/10.1080/02827588709382450
Avtzis DN, Petsopoulos D, Memtsas GI et al (2018) Revisiting the distribution of Thaumetopoea pityocampa (Lepidoptera: Notodontidae) and T. pityocampa ENA Clade in Greece. J Econ Entomol 111(3):1256–1260. https://doi.org/10.1093/jee/toy047
Axelson JN, Smith DJ, Daniels LD et al (2015) Multicentury reconstruction of western spruce budworm outbreaks in central British Columbia, Canada. Forest Ecol Manag 335:235–248. https://doi.org/10.1016/j.foreco.2014.10.002
Ayres MP, MacLean SF (1987) Development of birch leaves and the growth energetics of Epirrita autumnata (Geometridae). Ecology 68(3):558–568. https://doi.org/10.2307/1938461
Balch RE (1939) The outbreak the European spruce sawfly in Canada and some important features of its bionomics. J Econ Entomol 32(3):412–418. https://doi.org/10.1093/jee/32.3.412
Baltensweiler W (1993a) Why the larch bud-moth cycle collapsed in the subalpine larch-cembran pine forests in the year 1990 for the first time since 1850. Oecologia 94:62–66. https://doi.org/10.1007/BF00317302
Baltensweiler W (1993b) A contribution to the explanation of the larch bud moth cycle, the polymorphic fitness hypothesis. Oecologia 93:251–255. https://doi.org/10.1007/BF00317678
Baltensweiler W, Fischlin A (1988) The larch budmoth in the Alps. In: Berryman AA (ed) Dynamics of forest insect populations. Springer, MA, pp 331–351. https://doi.org/10.1007/978-1-4899-0789-9_17
Baltensweiler W, Benz G, Bovey P et al (1977) Dynamics of larch bud moth populations. Annu Rev Entomol 22:79–100. https://doi.org/10.1146/annurev.en.22.010177.000455
Baranchikov YN, Sukachev VN (1989) Ecological basis of the evolution of host relationships in Eurasian gypsy moth populations. USDA NE GTR 123:319–338
Barbehenn RV, Constabel CP (2011) Tannins in plant-herbivore interactions. Phytochemistry 72(13):1551–1565. https://doi.org/10.1016/j.phytochem.2011.01.040
Battisti A (1988) Host-plant relationships and population dynamics of the pine processionary caterpillar Thaumetopoea pityocampa (Denis & Schiffermuller). J App Entomol 105(1–5):393–402. https://doi.org/10.1111/j.1439-0418.1988.tb00202.x
Battisti A, Stastny M, Netherer S et al (2005) Expansion of geographic range in the pine processionary moth caused by increased winter temperatures. Ecol Appl 15(6):2084–2096. https://doi.org/10.1890/04-1903
Battisti A, Stastny M, Buffo E et al (2006) A rapid altitudinal range expansion in the pine processionary moth produced by the 2003 climatic anomaly. Global Change Biol 12(4):662–671. https://doi.org/10.1111/j.1365-2486.2006.01124.x
Beckwith RC (1976) Influence of host foliage on the Douglas-fir tussock moth. Environ Entomol 5(1):73–77. https://doi.org/10.1093/ee/5.1.73
Bejer B (1986) Outbreaks of Nun Moth (Lymantria monacha L) in Denmark with Remarks on their Control. Anz Schadlingskd Pfl 59:86–89. https://doi.org/10.1007/BF01903455
Belle-Isle J, Kneeshaw D (2007) A stand and landscape comparison of the effects of a spruce budworm (Choristoneura fumiferana (Clem.)) outbreak to the combined effects of harvesting and thinning on forest structure. Forest Ecol Manag 246(2–3):163–174. https://doi.org/10.1016/j.foreco.2007.03.038
Bellone D, Klapwijk MJ, Björkman C (2017) Habitat heterogeneity affects predation of European pine sawfly cocoons. Ecol Evol 7(24):11011–11020. https://doi.org/10.1002/ece3.3632
Berguet C, Martin M, Arseneault D et al (2021) Spatiotemporal Dynamics of 20th-Century Spruce Budworm Outbreaks in Eastern Canada: Three Distinct Patterns of Outbreak Severity. Dig Front Ecol Evol 8:544088. https://doi.org/10.3389/fevo.2020.544088
Berryman AA (1978) Population cycles of the Douglas-fir tussock moth (Lepidoptera: Lymantriidae): the time-delay hypothesis. Can Entomol 110(5):513–518. https://doi.org/10.4039/Ent110513-5
Bhattarai R, Rahimzadeh-Bajgiran P, Weiskittel A et al (2021) Spruce budworm tree host species distribution and abundance mapping using multi-temporal Sentinel-1 and Sentinel-2 satellite imagery. ISPRS J Photogram Remote Sens 172:28–40. https://doi.org/10.1016/j.isprsjprs.2020.11.023
Bittner TD, Hajek AE, Liebhold AM et al (2017) Modification of a pollen trap design to capture airborne conidia of Entomophaga maimaiga and detection by quantitative PCR. Appl Environ Microbiol 83(17):1–11. https://doi.org/10.1128/AEM.00724-17
Bjørnstad ON (2000) Cycles and synchrony: two historical ‘experiments’ and one experience. J Anim Ecol 69(5):869–873. https://www.jstor.org/stable/2647407. Accessed 18 October 2022
Bjørnstad ON, Ims RA, Lambin X (1999) Spatial population dynamics: analyzing patterns and processes of population synchrony. Trends Ecol Evol 14(11):427–432. https://doi.org/10.1016/S0169-5347(99)01677-8
Bjørnstad ON, Peltonen M, Liebhold AM et al (2002) Waves of larch budmoth outbreaks in the European Alps. Science 298(5595):1020–1023. https://doi.org/10.1126/science.1075182
Bjørnstad ON, Liebhold AM, Johnson DM (2008) Transient synchronization following invasion: revisiting Moran’s model and a case study. Popul Ecol 50(4):379–389. https://doi.org/10.1007/s10144-008-0105-5
Bjørnstad ON, Robinet C, Liebhold AM (2010) Geographic variation in North American gypsy moth cycles: subharmonics, generalist predators, and spatial coupling. Ecology 91(1):106–118. https://doi.org/10.1890/08-1246.1
Blair CP (1979) Browntail moth, its caterpillar and their rash. Clin Exp Dermatol 4(2):215–222. https://doi.org/10.1111/j.1365-2230.1979.tb01621.x
Boettner GH, Elkinton JS, Boettner CJ (2000) Effects of a biological control introduction on three nontarget native species of saturniid moths. Conserv Biol 14(6):1798–1806. https://doi.org/10.1111/j.1523-1739.2000.99193.x
Bouchard M, Régnière J, Therrien P (2018a) Bottom-up factors contribute to large-scale synchrony in spruce budworm populations. Can J for Res 48(3):277–284. https://doi.org/10.1139/cjfr-2017-0051
Bouchard M, Martel V, Régnière J et al (2018b) Do natural enemies explain fluctuations in low-density spruce budworm populations? Ecology 99(9):2047–2057. https://doi.org/10.1002/ecy.2417
Boulanger Y, Arseneault D, Morin H et al (2012) Dendrochronological reconstruction of spruce budworm (Choristoneura fumiferana) outbreaks in southern Quebec for the last 400 years. Can J for Res 42(7):1264–1276. https://doi.org/10.1139/x2012-069
Boyd KS, Drummond F, Donahue C et al (2021) Factors influencing the population fluctuations of Euproctis chrysorrhoea (Lepidoptera: Erebidae) in Maine. Environ Entomol 50(5):1203–1216. https://doi.org/10.1093/ee/nvab060
Broadley HJ (2018) Impact of native natural enemies on populations of the invasive winter moth, (Operophtera brumata L) in the northeast United States. Dissertation, University of Massachusetts.https://doi.org/10.7275/12760419
Broadley HJ, Boucher M, Burand JP et al (2017) The phylogenetic relationship and cross-infection of nucleopolyhedroviruses between the invasive winter moth (Operophtera brumata) and its native congener, Bruce spanworm (O. bruceata). J Invertebr Pathol 143:61–68. https://doi.org/10.1016/j.jip.2016.11.016
Broadley HJ, Kula RR, Boettner GH et al (2019) Recruitment of native parasitic wasps to populations of the invasive winter moth in the northeastern United States. Biol Invasions 21:2871–2890. https://doi.org/10.1007/s10530-019-02019-4
Broadley HJ, Boettner GH, Schneider B et al (2022) Native generalist natural enemies and an introduced specialist parasitoid together control an invasive forest insect. Dig Ecol Appl. https://doi.org/10.1002/eap.2697
Brookes MH, Stark RW, Campbell RW (eds) (1978) The Douglas-fir tussock moth: a synthesis. USDA, Washington
Brown CE (1962) The life history and dispersal of the Bruce Spanworm, Operophtera bruceata. Can Entomol 94(10):1103‒1107.https://doi.org/10.4039/Ent941103-10
Brown JH, Halliwell DB, Gould WP (1979) Gypsy moth defoliation: impact in Rhode Island forests. J for 77(1):30–32. https://doi.org/10.1093/jof/77.1.30
Brown RC (1931) Observations on the satin moth and its natural enemies in Central Europe. USDA Circular 176
Büntgen U, Liebhold A, Nievergelt D et al (2020) Return of the moth: rethinking the effect of climate on insect outbreaks. Oecologia 192:543–552. https://doi.org/10.1007/s00442-019-04585-9
Burand JP, Kim W, Welch A et al (2011) Identification of a nucleopolyhedrovirus in winter moth populations from Massachusetts. J Invertebr Pathol 108(3):217–219. https://doi.org/10.1016/j.jip.2011.08.005
Burgess AF (1921) The satin moth: an introduced enemy of poplars and willows. USDA Circular 167
Burgess AF, Crossman SS (1927) The Satin Moth, a recently introduced pest. USDA Bulletin 1469. https://www.biodiversitylibrary.org/bibliography/107926. Accessed 18 October 2022
Butt C, Quiring D, Hébert C et al (2010) Influence of balsam fir (Abies balsamea) budburst phenology on hemlock looper (Lambdina fiscellaria). Entomol Exp Appl 134(3):220–226. https://doi.org/10.1111/j.1570-7458.2009.00963.x
Cadogan BL, Scharbach RD, Krause RE et al (2018) Linkages between the phenologies of jack pine (Pinus banksiana) foliage and jack pine budworm (Lepidoptera: Tortricidae). Great Lakes Entomol 38(1&2):58–75. https://scholar.valpo.edu/tgle/vol38/iss1/7. Accessed 18 October 2022
Camarero JJ, Tardif J, Gazol A et al (2022) Pine processionary moth outbreaks cause longer growth legacies than drought and are linked to the North Atlantic Oscillation. Sci Total Environ 819:153041. https://doi.org/10.1016/j.scitotenv.2022.153041
Campbell R, Smith DJ, Arsenault A (2006) Multicentury history of western spruce budworm outbreaks in interior Douglas-fir forests near Kamloops, British Columbia. Can J Forest Res 36(7):1758‒1769.https://doi.org/10.1139/x06-069
Campbell RW (1975) The gypsy moth and its natural enemies. USDA Bulletin 381. https://doi.org/10.22004/ag.econ.309219
Campbell RW (1993) Population dynamics of the major North American needle-eating budworms. USDA PNW-RP-463
Campbell RW, Podgwaite JD (1971) The disease complex of the gypsy moth. I. Major components. J Invertebr Pathol 18(1):101‒107.https://doi.org/10.1016/0022-2011(91)90015-I
Campbell RW, Sloan RJ (1977) Forest stand responses to defoliation by the gypsy moth. For Sci 23(s2):1–34. https://academic.oup.com/forestscience/article-abstract/23/suppl_2/a0001/4675788?login=true. Accessed 18 October 2022
Campbell RW, Sloan RJ (1978a) Natural maintenance and decline of gypsy moth outbreaks. Environ Entomol 7(3):389–395. https://doi.org/10.1093/ee/7.3.389
Campbell RW, Sloan RJ (1978b) Numerical bimodality among North-American gypsy moth populations. Environ Entomol 7(5):641–646. https://doi.org/10.1093/ee/7.5.641
Campbell RW, Beckwith RC, Torgersen TR (1983) Numerical Behavior of some western spruce budworm (Lepidoptera: Tortricidae) populations in Washington and Idaho. Environ Entomol 12(5):1366. https://doi.org/10.1093/ee/12.5.1360
Canning EU (1960) Two new microsporidian parasites of the winter moth, Operophtera brumata (L). J Parasitol 46(6):755–763. https://doi.org/10.2307/3275526
Canning EU, Wigley PJ, Barker RJ (1983) The taxonomy of three species of microsporidia (Protozoa: Microspora) from an oakwood population of winter moths Operophtera brumata (L.) (Lepidoptera: Geometridae). Sys Parasitol 5:147–159. https://doi.org/10.1007/BF00049242
Cardé RT, Minks AK (1995) Control of moth pests by mating disruption: successes and constraints. Annu Rev Entomol 40:559–585. https://www.annualreviews.org/doi/abs/10.1146/annurev.en.40.010195.003015. Accessed 18 October 2022
Carlisle A, Brown AHF, White EJ (1966) Litter fall, leaf production and the effects of defoliation by Tortrix viridana in a sessile oak (Quercus petraea) woodland. J Ecol 54(1):65–85. https://doi.org/10.2307/2257659
Carus S (2004) Impact of defoliation by the pine processionary moth (Thaumetopoea pityocampa) on radial, height and volume growth of Calabrian pine (Pinus brutia) trees in Turkey. Phytoparasitica 32:459–469. https://doi.org/10.1007/BF02980440
Carus S (2010) Effect of defoliation by the pine processionary moth (PPM) on radial, height and volume growth of Crimean pine (Pinus nigra) trees in Turkey. J Environ Biol 31(4):453–460. https://pubmed.ncbi.nlm.nih.gov/21186719/. Accessed 18 October 2022
Castagneyrol B, Jactel H, Brockerhoff EG et al (2016) Host range expansion is density dependent. Oecologia 182:779–788. https://doi.org/10.1007/s00442-016-3711-5
Cayuela L, Hernández R, Hódar JA et al (2014) Tree damage and population density relationships for the pine processionary moth: Prospects for ecological research and pest management. Forest Ecol Manag 328:319–325. https://doi.org/10.1016/j.foreco.2014.05.051
Chang WY, Lantz VA, Hennigar CR et al (2012) Economic impacts of forest pests: a case study of spruce budworm outbreaks and control in New Brunswick, Canada. Can J Forest Res 42(3):490‒505.https://doi.org/10.1139/x11-190
Charbonneau D, Lorenzetti F, Doyon F et al (2012) The influence of stand and landscape characteristics on forest tent caterpillar (Malacosoma disstria) defoliation dynamics: the case of the 1999–2002 outbreak in northwestern Quebec. Can J Forest Res 42(10):1827–1836. https://doi.org/10.1139/x2012-126
Chen Z, Kolb TE, Clancy KM (2001) Mechanisms of Douglas-fir resistance to western spruce budworm defoliation: bud burst phenology, photosynthetic compensation and growth rate. Tree Physiol 21(16):1159–1169. https://doi.org/10.1093/treephys/21.16.1159
Chen Z, Kolb TE, Clancy KM (2002) The role of monoterpenes in resistance of Douglas fir to western spruce budworm defoliation. J Chem Ecol 28(5):897–920. https://doi.org/10.1023/A:1015297315104
Chorbadjian RA, Phelan PL, Herms DA (2019) Tight insect-host phenological synchrony constrains the life-history strategy of European pine sawfly. Agric for Entomol 21(1):15–27. https://doi.org/10.1111/afe.12299
Ciesla WM (1964a) Egg Parasites of Elm Spanworm in Southern Appalachian Mountains. J Econ Entomol 57(6):837–838. https://doi.org/10.1093/jee/57.6.837
Ciesla WM (1964b) Life history and habits of the elm spanworm, Ennomos subsignarius, in the southern Appalachian Mountains (Lepidoptera: Geometridae). Ann Entomol Soc Am 57(5):591–596. https://doi.org/10.1093/aesa/57.5.591
Clancy KM, Giese RL, Benjamin DM (1980) Predicting jack-pine budworm infestations in northwestern Wisconsin. Environ Entomol 9(6):743–751. https://doi.org/10.1093/ee/9.6.743
Clancy KM, Itami JK, Huebner DP (1993) Douglas-Fir nutrients and terpenes: potential resistance factors to western spruce budworm defoliation. For Sci 39(1):78–94. https://academic.oup.com/forestscience/article-abstract/39/1/78/4627128. Accessed 18 October 2022
Clancy KM, Chen Z, Kolb TE (2004) Foliar nutrients and induced susceptibility: genetic mechanisms of Douglas-fir resistance to western spruce budworm defoliation. Can J Forest Res 34(4):939–949. https://doi.org/10.1139/x03-264
Cooke BJ, Roland J (2000) Spatial analysis of large-scale patterns of forest tent caterpillar outbreaks. Ecoscience 7(4):410–422. https://doi.org/10.1080/11956860.2000.11682611
Cooke BJ, Roland J (2003) The effect of winter temperature on forest tent caterpillar (Lepidoptera: Lasiocampidae) egg survival and population dynamics in northern climates. Environ Entomol 32(2):299–311. https://doi.org/10.1603/0046-225X-32.2.299
Cooke BJ, MacQuarrie CJK, Lorenzetti F (2012) The dynamics of forest tent caterpillar outbreaks across east-central Canada. Ecography 35(5):422–435. https://doi.org/10.1111/j.1600-0587.2011.07083.x
Cooke BJ, Sturtevant BR, Robert LE (2022) The forest tent caterpillar in Minnesota: detectability, impact, and cycling dynamics. Forests 13(4):601. https://doi.org/10.3390/f13040601
Cooper D, Cory JS, Theilmann DA et al (2003) Nucleopolyhedroviruses of forest and western tent caterpillars: cross-infectivity and evidence for activation of latent virus in high-density field populations. Ecol Entomol 28(1):41–50. https://doi.org/10.1046/j.1365-2311.2003.00474.x
Cory JS, Hirst ML, Sterling PA et al (2000) Narrow host range nucleopolyhedrovirus for control of the browntail moth (Lepidoptera: Lymantriidae). Environ Entomol 29(3):661–667. https://doi.org/10.1603/0046-225X-29.3.661
Crawford HS, Jennings DT (1989) Predation by birds on spruce budworm Choristoneura fumiferana: functional, numerical, and total responses. Ecology 70(1):152–163. https://doi.org/10.2307/1938422
Dahlsten DL, Luck RF, Schlinger EI et al (1977) Parasitoids and predators of Douglas-Fir tussock moth, Orgyia pseudotsugata (Lepidoptera: Lymantridae), in low to moderate populations in central California. Can Entomol 109(5):727–746. https://doi.org/10.4039/Ent109727-5
Daniel CJ, Myers JH (1995) Climate and outbreaks of the forest tent caterpillar. Ecography 18(4):353–362. https://doi.org/10.1111/j.1600-0587.1995.tb00138.x
Davidson CB, Gottschalk KW, Johnson JE (1999) Tree mortality following defoliation by the European gypsy moth (Lymantria dispar L.) in the United States: A Review. For Sci 45(1):74–84. https://doi.org/10.1093/forestscience/45.1.74
Delisle J, Labrecque A, Royer L et al (2013) Impact of short-term exposure to low subzero temperatures on egg hatch in the hemlock looper, Lambdina fiscellaria. Entomol Exp Appl 149(3):206‒218.https://doi.org/10.1111/eea.12123
Delisle J, Bernier-Cardou M, Laroche G (2016) Reproductive performance of the hemlock looper, Lambdina fiscellaria, as a function of temperature and population origin. Entomol Exp Appl 161(3):219–231. https://doi.org/10.1111/eea.12469
Delvas N, Bauce É, Labbé C et al (2011) Phenolic compounds that confer resistance to spruce budworm. Entomol Exp Appl 141(1):35–44. https://doi.org/10.1111/j.1570-7458.2011.01161.x
Din Q (2021) Dynamics and chaos control for a novel model incorporating plant quality index and larch budmoth interaction. Chaos Solitons Fractals 153(2):111595. https://doi.org/10.1016/j.chaos.2021.111595
Donahue KL, Broadley HJ, Elkinton JS et al (2019) Using the SSU, ITS, and Ribosomal DNA Operon arrangement to characterize two microsporidia infecting bruce spanworm, Operophtera bruceata (Lepidoptera: Geometridae). J Eukaryotic Microbiol 66(3):424–434. https://doi.org/10.1111/jeu.12685
Donovan SD, MacLean DA, Zhang Y et al (2021) Evaluating annual spruce budworm defoliation using change detection of vegetation indices calculated from satellite hyperspectral imagery. Remote Sens Environ 253:112204. https://doi.org/10.1016/j.rse.2020.112204
Dormont L, Baltensweiler W, Choquet R et al (2006) Larch- and pine-feeding host races of the larch bud moth (Zeiraphera diniana) have cyclic and synchronous population fluctuations. Oikos 115(2):299–307. https://doi.org/10.1111/j.2006.0030-1299.15010.x
Doucette CF (1954) Recurrence of the Satin Moth in the Pacific Northwest. J Econ Entomol 47(5):939–940. https://doi.org/10.1093/jee/47.5.939
Dowden PB (1939) Present status of the European spruce sawfly, Diprion polytomum (Htg.), in the United States. J Econ Entomol 32(5):619–624. https://academic.oup.com/jee/article-abstract/32/5/619/798754?redirectedFrom=fulltext. Accessed 18 October 2022
Drever MC, Smith AC, Venier LA et al (2018) Cross-scale effects of spruce budworm outbreaks on boreal warblers in eastern Canada. Ecol Evol 8(15):7334–7345. https://doi.org/10.1002/ece3.4244
Drooz AT, Ghent JH, Huber CM (1985) Insect parasites associated with the Introduced pine Sawfly, Diprion-similis (Hartig) (Hymenoptera: Diprionidae), in North-Carolina. Environ Entomol 14(4):401‒403.https://doi.org/10.1093/ee/14.4.401
Du Merle P (1983) Mortality factors for the eggs of Tortrix viridana L (Lep. Tortricidae) 3. Regulatory action of each factor and examination of total mortality [green oak tortrix; predation, parasitism, disease; Southern France]. Agronomie 3(5):429–434. https://agris.fao.org/agris-search/search.do?recordID=XE8436337. Accessed 18 October 2022
Dwyer G, Dushoff J, Yee SH (2004) The combined effects of pathogens and predators on insect outbreaks. Nature 430:341–345. https://doi.org/10.1038/nature02569
Eidt DC, Embree DG, Smith CC (1966) Distinguishing adults of the winter moth Operophtera brumata (L.), and Bruce spanworm O. bruceata (Hulst) (Lepidoptera: Geometridae). Can Entomol 98(3):258–261. https://doi.org/10.4039/Ent98258-3
Elkinton JS, Boettner GH (2012) Benefits and harm caused by the introduced generalist tachinid, Compsilura concinnata, in North America. Biocontrol 57:277–288. https://doi.org/10.1007/s10526-011-9437-8
Elkinton JS, Liebhold AM (1990) Population dynamics of gypsy moth in North America. Annu Rev Entomol 35:571–596. https://doi.org/10.1146/annurev.en.35.010190.003035
Elkinton JS, Hajek AE, Boettner GH et al (1991) Distribution and apparent spread of Entomophaga maimaiga (Zygomycetes: Entomophthorales) in gypsy moth (Lepidoptera: Lymantriidae) populations in North America. Environ Entomol 20(6):1601–1605. https://doi.org/10.1093/ee/20.6.1601
Elkinton JS, Healy WM, Buonaccorsi JP et al (1996) Interactions among gypsy moths, White-footed mice, and acorns. Ecology 77(8):2332–2342. https://doi.org/10.2307/2265735
Elkinton JS, Liebhold AM, Muzika RM (2004) Effects of alternative prey on predation by small mammals on gypsy moth pupae. Popul Ecol 46:171–178. https://doi.org/10.1007/s10144-004-0175-y
Elkinton JS, Parry D, Boettner GH (2006) Implicating an introduced generalist parasitoid in the invasive browntail moth’s enigmatic demise. Ecology 87(10):2664–2672. https://doi.org/10.1890/0012-9658(2006)87[2664:IAIGPI]2.0.CO;2
Elkinton JS, Preisser E, Boettner G et al (2008) Factors influencing larval survival of the invasive Browntail moth (Lepidoptera: Lymantriidae) in relict North American populations. Environ Entomol 37(6):1429–1437. https://doi.org/10.1603/0046-225X-37.6.1429
Elkinton JS, Boettner GH, Sermac M et al (2010) Survey for Winter moth (Lepidoptera: Geometridae) in northeastern North America with pheromone-baited traps and hybridization with the native Bruce spanworm (Lepidoptera: Geometridae). Ann Entomol Soc Am 103(2):135–145. https://doi.org/10.1603/AN09118
Elkinton JS, Liebhold A, Boettner GH et al (2014) Invasion spread of Operophtera brumata in northeastern United States and hybridization with O. bruceata. Biol Invasions 16:2263–2272. https://doi.org/10.1007/s10530-014-0662-9
Elkinton JS, Boettner GH, Broadley HJ et al (2018) Biological control of the winter moth in the northeastern North America. USDA FHAAST-2018-03. 8p. https://www.fs.usda.gov/foresthealth/publications/fhaast/index.shtml. Accessed 19 October 2022
Elkinton JS, Bittner TD, Pasquarella VJ et al (2019) Relating aerial deposition of Entomophaga maimaiga Conidia (Zoopagomycota: Entomophthorales) to mortality of Gypsy moth (Lepidoptera: Erebidae) larvae and nearby defoliation. Environ Entomol 48(5):1214–1222. https://doi.org/10.1093/ee/nvz091
Elkinton JS, Boettner GH, Broadley HJ (2021) Successful biological control of winter moth, Operophtera brumata, in the northeastern United States. J Ecol Appl 31(5):e02326. https://doi.org/10.1002/eap.2326
Embree DG (1965) The population dynamics of the winter moth in Nova Scotia, 1954–1962. Mem Entomol Soc Can 97(S46):5–57. https://doi.org/10.4039/entm9746fv
Embree DG (1966) The role of introduced parasites in the control of the winter moth in Nova Scotia. Can Entomol 98(11):1159–1168. https://doi.org/10.4039/Ent981159-11
Embree DG (1967) Effects of winter moth on growth and mortality of red oak in Nova Scotia. For Sci 13(3):295–299. https://academic.oup.com/forestscience/article-abstract/13/3/295/4709561. Accessed 19 October 2022
Esper J, Büntgen U, Frank DC et al (2007) 1200 years of regular outbreaks in alpine insects. P Roy Soc B-Biol Sci 274:671–679. https://doi.org/10.1098/rspb.2006.0191
Fält-Nardmann JJJ, Ruohomäki K, Tikkanen O-P et al (2018a) Cold hardiness of Lymantria monacha and L. dispar (Lepidoptera: Erebidae) eggs to extreme winter temperatures: implications for predicting climate change impacts. Ecol Entomol 43(4):422–430. https://doi.org/10.1111/een.12515
Fält-Nardmann JJJ, Klemola T, Ruohomäki K et al (2018b) Local adaptations and phenotypic plasticity may render gypsy moth and nun moth future pests in northern European boreal forests. Can J Forest Res 48(3):265–276. https://doi.org/10.1139/cjfr-2016-0481
Fält-Nardmann JJJ, Tikkanen O-P, Ruohomäki K et al (2018c) The recent northward expansion of Lymantria monacha in relation to realised changes in temperatures of different seasons. Forest Ecol Manag 427:96–105. https://doi.org/10.1016/j.foreco.2018.05.053
Fahrner SJ, Albers JS, Albers MA et al (2016) Oviposition and feeding on red pine by jack pine budworm at a previously unrecorded scale. Agric for Entomol 18(3):214–222. https://doi.org/10.1111/afe.12154
Fedde GF (1965) The popular and scientific nomenclature of the Elm Spanworm, Ennomos subsignarius (Lepidoptera: Geometridae). Ann Entomol Soc Am 58(1):68–71. https://doi.org/10.1093/aesa/58.1.68
Feeny P (1970) Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology 51(4):565–581. https://doi.org/10.2307/1934037
Fisher GT (1970) Parasites and predators of species of a saddled prominent complex at Groton, Vermont. J Econ Entomol 63(5):1613‒1614.https://doi.org/10.1093/jee/63.5.1613
Fiske WF, Burgess AF (1910) The natural control of Heterocampa guttivitta. J Econ Entomol 3(5):389–394. https://doi.org/10.1093/jee/3.5.389
Flower A (2016) Three centuries of synchronous forest defoliator outbreaks in western North America. PLoS ONE 11(10):e0164737. https://doi.org/10.1371/journal.pone.0164737
Flower A, Gavin DG, Heyerdahl EK et al (2014a) Drought-triggered western spruce budworm outbreaks in the interior Pacific Northwest: A multi-century dendrochronological record. For Ecol Manag 324:16–27. https://doi.org/10.1016/j.foreco.2014.03.042
Flower A, Gavin DG, Heyerdahl EK et al (2014b) Western spruce budworm outbreaks did not increase fire risk over the last three centuries: a dendrochronological analysis of inter-disturbance synergism. PLoS ONE 9(12):e114282. https://doi.org/10.1371/journal.pone.0114282
Frago E, Guara M, Pujade-Villar J et al (2010) Winter feeding leads to a shifted phenology in the browntail moth Euproctis chrysorrhoea on the evergreen strawberry tree Arbutus unedo. Agric for Entomol 12(4):381–388. https://doi.org/10.1111/j.1461-9563.2010.00489.x
Frago E, Pujade-Villar J, Guara M et al (2011) Providing insights into browntail moth local outbreaks by combining life table data and semi-parametric statistics. Ecol Entomol 36(2):188–199. https://doi.org/10.1111/j.1365-2311.2010.01259.x
Frago E, Pujade-Villar J, Guara M et al (2012) Hyperparasitism and seasonal patterns of parasitism as potential causes of low top-down control in Euproctis chrysorrhoea L. (Lymantriidae). Biol Control 60(2):123–131. https://doi.org/10.1016/j.biocontrol.2011.11.013
Frank JH (1967) The insect predators of the pupal stage of the winter moth, Operophtera brumata (L) (Lepidoptera: Hydriomenidae). J Anim Ecol 36(2):375–389. https://doi.org/10.2307/2920
Fry HRC, Quiring DT, Ryall KL et al (2008) Relationships between elm spanworm, Ennomos subsignaria, juvenile density and defoliation on mature sycamore maple in an urban environment. Forest Ecol Manag 255(7):2726–2732. https://doi.org/10.1016/j.foreco.2008.01.039
Fry HRC, Quiring DT, Ryall KL et al (2009) Influence of intra-tree variation in phenology and oviposition site on the distribution and performance of Ennomos subsignaria on mature sycamore maple. Ecol Entomol 34(3):394–405. https://doi.org/10.1111/j.1365-2311.2009.01091.x
Fuentealba A, Pureswaran D, Bauce É et al (2017) How does synchrony with host plant affect the performance of an outbreaking insect defoliator? Oecologia 184:847–857. https://doi.org/10.1007/s00442-017-3914-4
Fuester RW, Hajek AE, Elkinton JS et al (2014) Gypsy moth (Lymantria dispar L.) (Lepidoptera: Erebidae: Lymantriinae). In: Van Driesche R, Reardon R (eds) The use of classical biological control to preserve forests in North America. USDA FHET-2013 2:49–82. https://bugwoodcloud.org/resource/files/14888.pdf. Accessed 19 October 2022
Gansner DA, Arner SL, Widmann RH et al (1993) After two decades of gypsy moth, is there any oak left? North J Appl for 10(4):184–186. https://doi.org/10.1093/njaf/10.4.184
Georgiev G, Hubenov Z, Mirchev P et al (2022) New tachinid parasitoids on pine processionary moth (Thaumetopoea pityocampa) (Diptera: Tachinidae) in Bulgaria. Silva Balcanica 23(1):5–10. https://doi.org/10.3897/silvabalcanica.23.e81890
Germain M, Kneeshaw D, De Grandpré L et al (2021) Insectivorous songbirds as early indicators of future defoliation by spruce budworm. Landscape Ecol 36(10):3013–3027. https://doi.org/10.1007/s10980-021-01300-z
Ghirardo A, Heller W, Fladung M et al (2012) Function of defensive volatiles in pedunculate oak (Quercus robur) is tricked by the moth Tortrix viridana. Plant Cell Environ 35(12):2192–2207. https://doi.org/10.1111/j.1365-3040.2012.02545.x
Gillespie DR, Finlayson T, Tonks NV et al (1978) Occurrence of the winter moth, Operophtera brumata (Lepidoptera: Geometridae), on southern Vancouver Island, British Columbia. Can Entomol 110(2):223‒224.https://doi.org/10.4039/Ent110223-2
Gilligan TM, Brown JW (2014) A new name for the western spruce budworm (Lepidoptera: Tortricidae)? Can Entomol 146(6):583–589. https://doi.org/10.4039/tce.2014.17
Goodbody TRH, Coops NC, Hermosilla T et al (2018) Digital aerial photogrammetry for assessing cumulative spruce budworm defoliation and enhancing forest inventories at a landscape-level. ISPRS J Photogramm 142:1–11. https://doi.org/10.1016/j.isprsjprs.2018.05.012
Gray DR (2018) Age-dependent developmental response to temperature: an examination of the rarely tested phenomenon in two species (gypsy moth (Lymantria dispar) and winter moth (Operophtera brunata)). InSects 9(2):41. https://doi.org/10.3390/insects9020041
Gur’yanova TM (2006) Fecundity of the European pine sawfly Neodiprion sertifer (Hymenoptera, Diprionidae) related to cyclic outbreaks: invariance effects. Entomol Rev 86:910–921. https://doi.org/10.1134/S0013873806080069
Gwiazdowski RA, Elkinton JS, Dewaard JR et al (2013) Phylogeographic diversity of the winter moths Operophtera brumata and O. bruceata (Lepidoptera: Geometridae) in Europe and North America. Ann Entomol Soc Am 106(2):143–151. https://doi.org/10.1603/AN12033
Habermann M (2000) The larch casebearer and its host tree: I. Population dynamics of the larch casebearer (Coleophora laricella Hbn.) from latent to outbreak density in the field. Forest Ecol Manag 136(1–3):11–22. https://doi.org/10.1016/S0378-1127(99)00266-2
Hajek AE (1997) Fungal and viral epizootics in gypsy moth (Lepidoptera: Lymantriidae) populations in central New York. Biol Control 10(1):58–68. https://doi.org/10.1006/bcon.1997.0541
Hajek AE (1999) Pathology and epizootiology of Entomophaga maimaiga infections in forest Lepidoptera. Microbiol Mol Biol R 63(4):814–835. https://doi.org/10.1128/MMBR.63.4.814-835.1999
Hajek AE (2007) Introduction of a fungus into North America for control of gypsy moth. In: Vincent C, Goettel MS, Lazarovits G (eds) Biological control: a global perspective: case studies from around the world, CABI, Cambridge, MA, pp 53–62. https://doi.org/10.1079/9781845932657.0053
Hajek AE, Tobin PC (2010) Micro-managing arthropod invasions: eradication and control of invasive arthropods with microbes. Biol Invasions 12:2895–2912. https://doi.org/10.1007/s10530-010-9735-6
Hajek AE, Carruthers RI, Soper RS (1990a) Temperature and moisture relations of sporulation and germination by Entomophaga-maimaiga (Zygomycetes: Entomophthoraceae), a fungal pathogen of Lymantria dispar (Lepidoptera: Lymantriidae). Environ Entomol 19(1):85–90. https://doi.org/10.1093/ee/19.1.85
Hajek AE, Humber RA, Elkinton JS et al (1990b) Allozyme and restriction fragment length polymorphism analyses confirm Entomophaga maimaiga responsible for 1989 epizootics in North American gypsy moth populations. P Natl Acad Sci USA 87(18):6979–6982. https://doi.org/10.1073/pnas.87.18.6979
Hajek AE, Elkinton JS, Witcosky JJ (1996) Introduction and spread of the fungal pathogen Entomophaga maimaiga (Zygomycetes: Entomophthorales) along the leading edge of gypsy moth (Lepidoptera: Lymantriidae) spread. Environ Entomol 25(5):1235–1247. https://doi.org/10.1093/ee/25.5.1235
Hajek AE, Tobin PC, Haynes KJ (2015) Replacement of a dominant viral pathogen by a fungal pathogen does not alter the collapse of a regional forest insect outbreak. Oecologia 177:785–797. https://doi.org/10.1007/s00442-014-3164-7
Hajek AE, Gardescu S, Delalibera I (2020) Summary of classical biological control introductions of entomopathogens and nematodes for insect control. Biocontrol 66:1671–2180. https://doi.org/10.1007/s10526-020-10046-7
Hall RJ, Skakun RS, Arsenault EJ (2006) Remotely sensed data in the mapping of insect defoliation. In: Wulder MA, Franklin SE (eds) Understanding forest disturbance and spatial pattern: remote sensing and GIS approaches, Taylor & Francis, Boca Raton, FL, pp 85–111. https://www.researchgate.net/publication/238730970. Accessed 19 October 2022
Hartl-Meier C, Esper J, Liebhold A et al (2017) Effects of host abundance on larch budmoth outbreaks in the European Alps. Agric for Entomol 19(4):376–387. https://doi.org/10.1111/afe.12216
Hassell MP (1968) Behavioural response of a tachinid fly (Cyzenis albicans (Fall) to its host, the winter moth (Operophtera brumata (L)). J Anim Ecol 37(3):627–639. https://doi.org/10.2307/3079
Hassell MP (1969a) A study of mortality factors acting upon Cyzenis albicans (Fall), a tachinid parasite of the winter moth (Operophtera brumata (L)). J Anim Ecol 38(2):329–339. https://doi.org/10.2307/2774
Hassell MP (1969b) A population model for the interaction between Cyzenis albicans (Fall.) (Tachinidae) and Operophtera brumata (L.) (Geometridae) at Wytham, Berkshire. J Anim Ecol 38(3):567–576. https://doi.org/10.2307/3035
Hassell MP (1980) Foraging strategies, population models and biological control—a case study. J Anim Ecol 49(2):603–628. https://doi.org/10.2307/4267
Haukioja E (1991) Induction of defenses in trees. Annu Rev Entomol 36:25–42. https://doi.org/10.1146/annurev.en.36.010191.000325
Havill NP, Elkinton J, Andersen JC et al (2017) Asymmetric hybridization between non-native winter moth, Operophtera brumata (Lepidoptera: Geometridae), and native Bruce spanworm, Operophtera bruceata, in the Northeastern United States, assessed with novel microsatellites and SNPs. Bull Entomol Res 107(2):241–250. https://doi.org/10.1017/S0007485316000857
Hawboldt LS, Cuming FG (1950) Cankerworms and European winter moth in Nova Scotia. Bi-m Progr Rep For Insect Invest Dep Agric Can 6(1):1–2. https://afc-fr.cfsnet.nfis.org/fias/pdfs/afc/atlantic_bimonthly_1950-6(1-6).pdf. Accesed 18 October 2022
Haynes KJ, Liebhold AM, Johnson DM (2009a) Spatial analysis of harmonic oscillation of gypsy moth outbreak intensity. Oecologia 159:249–256. https://doi.org/10.1007/s00442-008-1207-7
Haynes KJ, Liebhold AM, Fearer TM et al (2009b) Spatial synchrony propagates through a forest food web via consumer-resource interactions. Ecology 90(11):2974–2983. https://doi.org/10.1890/08-1709.1
Haynes KJ, Bjørnstad ON, Allstadt AJ et al (2013) Geographical variation in the spatial synchrony of a forest-defoliating insect: isolation of environmental and spatial drivers. P Roy Soc B-Biol Sci 280:20122373. https://doi.org/10.1098/rspb.2012.2373
Haynes KJ, Liebhold AM, Bjørnstad ON et al (2018a) Geographic variation in forest composition and precipitation predict the synchrony of forest insect outbreaks. Oikos 127(4):634–642. https://doi.org/10.1111/oik.04388
Haynes KJ, Tardif JC, Parry D (2018b) Drought and surface-level solar radiation predict the severity of outbreaks of a widespread defoliating insect. Ecosphere 9(8):e02387. https://doi.org/10.1002/ecs2.2387
Hébert C, Berthiaume R, Dupont A et al (2001) Population collapses in a forecasted outbreak of Lambdina fiscellaria (Lepidoptera: Geometridae) caused by spring egg parasitism by Telenomus spp. (Hymenoptera: Scelionidae). Environ Entomol 30(1):37–43. https://doi.org/10.1603/0046-225X-30.1.37
Hengeveld R (1989) Dynamics of biological invasions. Chapman and Hall, London
Hentschel R, Möller K, Wenning A et al (2018) Importance of ecological variables in explaining population dynamics of three important pine pest insects. Front Plant Sci 9:1667. https://doi.org/10.3389/fpls.2018.01667
Hibbard EL, Elkinton JS (2015) Effect of spring and winter temperatures on winter moth (Geometridae: Lepidoptera) larval eclosion in the northeastern United States. Environ Entomol 44(3):798–807. https://doi.org/10.1093/ee/nvv006
Hódar JA, Castro J, Zamora R (2003) Pine processionary caterpillar Thaumetopoea pityocampa as a new threat for relict Mediterranean Scots pine forests under climatic warming. Biol Conserv 110(1):123–129. https://doi.org/10.1016/S0006-3207(02)00183-0
Hódar JA, Torres-Muros L, Zamora R et al (2015) No evidence of induced defence after defoliation in three pine species against an expanding pest, the pine processionary moth. Forest Ecol Manag 356:166–172. https://doi.org/10.1016/j.foreco.2015.07.022
Holling CS (1959) The components of predation as revealed by a study of small-mammal predation of the European pine sawfly. Can Entomol 91(5):293–320. https://doi.org/10.4039/Ent91293-5
Horstmann K (1977) Wood ants (Formica polyctena Foerster) as mortality factors in population dynamics of the oak tortrix Tortrix viridana L. Z Angew Entomol 82(4):421–435. https://www.cabdirect.org/cabdirect/abstract/19770548022. Accessed 20 October 2022
Hughes JS, Cobbold CA, Haynes K et al (2015) Effects of Forest Spatial Structure on Insect Outbreaks: Insights from a Host-Parasitoid Model. Dig Am Nat 185(5):E130-152. https://doi.org/10.1086/680860
Hummel S, Agee JK (2003) Western spruce budworm defoliation effects on forest structure and potential fire behavior. Northwest Science 77(2):159–169. https://hdl.handle.net/2376/807
Humphrey N (1996) Satin moth in British Columbia. PFC CFS Forest Pest Leaflet No 38:1–4. https://www.cabdirect.org/cabdirect/abstract/19971102190. Accessed 20 October 2022
Hunter MD (1998) Interactions between Operophtera brumata and Tortrix viridana on oak: new evidence from time-series analysis. Ecol Entomol 23(2):168–173. https://doi.org/10.1046/j.1365-2311.1998.00124.x
Ilyinykh A (2011) Analysis of the causes of declines in Western Siberian outbreaks of the nun moth Lymantria monacha. Biocontrol 56:123–131. https://doi.org/10.1007/s10526-010-9316-8
Iqbal J, MacLean DA, Kershaw JA Jr (2011) Impacts of hemlock looper defoliation on growth and survival of balsam fir, black spruce and white birch in Newfoundland, Canada. Forest Ecol Manag 261(6):1106‒1114.https://doi.org/10.1016/j.foreco.2010.12.037
Ivashov AV, Simchuk AP, Medvedkov DA (2001) Possible role of inhibitors of trypsin-like proteases in the resistance of oaks to damage by oak leafroller Tortrix viridana L. and gypsy moth Lymantria dispar L. Ecol Entomol 26:664–668. https://resjournals.onlinelibrary.wiley.com/doi/pdf/10.1046/j.1365-2311.2001.00362.x. Accessed 20 October 2022
Ives WGH (1984) Operophtera bruceata (Hulst), Bruce Spanworm (Lepidoptera: Geometridae). In: Kelleher JS, Hulme MA (eds) (1984) Biological control programmes against insects and weeds in Canada 1969–1980. CAB, Slough, England, pp 349–351.
Ives WGH, Cunningham JC (1980) Application of nuclear polyhedrosis virus to control Bruce spanworm (Lepidoptera: Geometridae). Can Entomol 112(7):741–744. https://doi.org/10.4039/Ent112741-7
Iyengar SV, Balakrishnan J, Kurths J (2016) Impact of climate change on larch budmoth cyclic outbreaks. Sci Rep 6:27845. https://doi.org/10.1038/srep27845
Jacquet J-S, Orazio C, Jactel H (2012) Defoliation by processionary moth significantly reduces tree growth: a quantitative review. Ann for Sci 69:857–866. https://doi.org/10.1007/s13595-012-0209-0
Jeger M, Bragard C, Caffier D et al (2018) Pest categorisation of Dendrolimus sibiricus. EFSA J 16(6):e05301. https://doi.org/10.2903/j.efsa.2018.5301
Jepsen JU, Hagen SB, Ims RA et al (2008) Climate change and outbreaks of the geometrids Operophtera brumata and Epirrita autumnata in subarctic birch forest: evidence of a recent outbreak range expansion. J Anim Ecol 77(2):257–264. https://doi.org/10.1111/j.1365-2656.2007.01339.x
Jepsen JU, Hagen SB, Hogda KA et al (2009a) Monitoring the spatio-temporal dynamics of geometrid moth outbreaks in birch forest using MODIS-NDVI data. Remote Sens Environ 113:1939–1947. https://scholar.google.ca/scholar?q=Monitoring+the+spatio-temporal+dynamics+of+geometrid+moth+outbreaks+in+birch+forest+using+MODIS-NDVI+data&hl=en&as_sdt=0&as_vis=1&oi=scholart. Accessed 20 October 2022
Jepsen JU, Hagen SB, Karlsen SR et al (2009b) Phase-dependent outbreak dynamics of geometrid moth linked to host plant phenology. Proc R Soc B-Biol Sci 276(1676):4119–4128. https://doi.org/10.1098/rspb.2009.1148
Jepsen JU, Kapari L, Hagen SB et al (2011) Rapid northwards expansion of a forest insect pest attributed to spring phenology matching with sub-Arctic birch. Global Change Biol 17(6):2071–2083. https://doi.org/10.1111/j.1365-2486.2010.02370.x
Jepsen JU, Vindstad OPL, Barraquand F et al (2016) Continental-scale travelling waves in forest geometrids in Europe: an evaluation of the evidence. J Anim Ecol 85(2):385–390. https://doi.org/10.1111/1365-2656.12444
Johnson DM, Liebhold AM, Bjørnstad ON (2006a) Geographical variation in the periodicity of gypsy moth outbreaks. Ecography 29(3):367–374. https://doi.org/10.1111/j.2006.0906-7590.04448.x
Johnson DM, Liebhold AM, Tobin PC et al (2006b) Allee effects and pulsed invasion by the gypsy moth. Nature 444:361–363. https://doi.org/10.1038/nature05242
Kamata N (2000) Population dynamics of the beech caterpillar, Syntypistis punctatella, and biotic and abiotic factors. Popul Ecol 42(3):267–278. https://doi.org/10.1007/PL00012005
Kamata N (2002) Outbreaks of forest defoliating insects in Japan, 1950–2000. Bull Entomol Res 92(2):109–117. https://doi.org/10.1079/BER2002159
Kaya HK, Anderson JF (1974) Collapse of elm spanworm outbreak in Connecticut: role of Ooencyrtus sp. Environ Entomol 3(4):659–663. https://doi.org/10.1093/ee/3.4.659
Keena MA (2003) Survival and development of Lymantria monacha (Lepidoptera: Lymantriidae) on North American and introduced Eurasian tree species. J Econ Entomol 96(1):43–52. https://doi.org/10.1093/jee/96.1.43
Keena MA, Côté MJ, Grinberg PS et al (2008) World distribution of female flight and genetic variation in Lymantria dispar (Lepidoptera: Lymantriidae). Environ Entomol 37(1):636–649. https://doi.org/10.1603/0046-225X(2008)37[636:WDOFFA]2.0.CO;2
Kegg JD (1967) Sampling techniques for predicting fall cankerworm defoliation. J Econ Entomol 60(3):889–890. https://doi.org/10.1093/jee/60.3.889
Kegg JD (1973) Oak mortality caused by repeated gypsy moth defoliations in New Jersey. J Econ Entomol 66(3):639–641. https://doi.org/10.1093/jee/66.3.639
Kelly PM, Sterling PH, Speight MR et al (1988) Preliminary spray trials of a nuclear polyhedrosis virus as a control agent for the brown-tail moth, Euproctis chrysorrhoea (L) (Lepidoptera: Lymantriidae). Bull Entomol Res 78(2):227–234. https://doi.org/10.1017/S0007485300012992
Kenis M, Kloosterman K (2001) European parasitoids of the pine false webworm (Acantholyda erythrocephala (L.)) and their potential for biological control in North America. USDA GTR NE-277:65–73. https://www.researchgate.net/publication/242313271_European_Parasitoids_of_the_Pine_False_Webworm_Acantholyda_erythrocephala_L_and_Their_Potential_for_Biological_Control_in_North_America
Kenis M, Hurley BP, Hajek AE et al (2017) Classical biological control of insect pests of trees: facts and figures. Biol Invasions 19:3401–3417. https://doi.org/10.1007/s10530-017-1414-4
Kerslake JE, Kruuk LEB, Hartley SE et al (1996) Winter moth (Operophtera brumata (Lepidoptera: Geometridae)) outbreaks on Scottish heather moorlands: effects of host plant and parasitoids on larval survival and development. Bull Entomol Res 86(2):155–164. https://doi.org/10.1017/S0007485300052391
Kharuk VI, Ranson KJ, Kozuhovskaya AG et al (2004) NOAA/AVHRR satellite detection of Siberian silkmoth outbreaks in eastern Siberia. Int J Remote Sens 25(24):5543–5555. https://doi.org/10.1080/01431160410001719858
Kharuk VI, Im ST, Yagunov MN (2018) Migration of the northern boundary of the Siberian silk moth. Contemp Probl Ecol 11:26–34. https://doi.org/10.1134/S1995425518010055
Kimberling DN, Miller JC, Penrose RL (1986) Distribution and parasitism of winter moth, Operophtera brumata (Lepidoptera: Geometridae), in western Oregon. Environ Entomol 15(5):1042–1046. https://doi.org/10.1093/ee/15.5.1042
Kirichenko NI, Baranchikov YN, Vidal S (2009) Performance of the potentially invasive Siberian moth Dendrolimus superans sibiricus on coniferous species in Europe. Agric for Entomol 11(3):247–254. https://doi.org/10.1111/j.1461-9563.2009.00437.x
Klapwijk MJ, Björkman C (2018) Mixed forests to mitigate risk of insect outbreaks. Scand J Forest Res 33(8):772–780. https://doi.org/10.1080/02827581.2018.1502805
Klapwijk MJ, Csóka G, Hirka A et al (2013) Forest insects and climate change: long-term trends in herbivore damage. Ecol Evol 3(12):4183–4196. https://doi.org/10.1002/ece3.717
Klemola N, Heisswolf A, Ammunét T et al (2009) Reversed impacts by specialist parasitoids and generalist predators may explain a phase lag in moth cycles: a novel hypothesis and preliminary field tests. Ann Zool Fenn 46(5):380–393. https://doi.org/10.5735/086.046.0504
Klemola N, Andersson T, Ruohomäki K et al (2010) Experimental test of parasitism hypothesis for population cycles of a forest lepidopteran. Ecology 91(9):2506–2513. https://doi.org/10.1890/09-2076.1
Klemola T, Ruohomäki K, Andersson T et al (2004) Reduction in size and fecundity of the autumnal moth, Epirrita autumnata, in the increase phase of a population cycle. Oecologia 141:47–56. https://doi.org/10.1007/s00442-004-1642-z
Klemola T, Andersson T, Ruohomäki K (2008) Fecundity of the autumnal moth depends on pooled geometrid abundance without a time lag: implications for cyclic population dynamics. J Anim Ecol 77(3):597–604. https://doi.org/10.1111/j.1365-2656.2008.01369.x
Klemola T, Andersson T, Ruohomäki K (2014) Delayed density-dependent parasitism of eggs and pupae as a contributor to the cyclic population dynamics of the autumnal moth. Oecologia 175:1211–1225. https://doi.org/10.1007/s00442-014-2984-9
Kollberg I, Bylund H, Schmidt A et al (2013) Multiple effects of temperature, photoperiod and food quality on the performance of a pine sawfly. Ecol Entomol 38(2):201–208. https://doi.org/10.1111/een.12005
Kollberg I, Bylund H, Huitu O et al (2014) Regulation of forest defoliating insects through small mammal predation: reconsidering the mechanisms. Oecologia 176:975–983. https://doi.org/10.1007/s00442-014-3080-x
Kosunen M, Kantola T, Starr M et al (2016) Influence of soil and topography on defoliation intensity during an extended outbreak of the common pine sawfly (Diprion pini L.). IForest 10(1):164–171. https://doi.org/10.3832/ifor2069-009
Kouki J, Lyytikäinen-Saarenmaa P, Henttonen H et al (1998) Cocoon predation on diprionid sawflies: the effect of forest fertility. Oecologia 116:482–488. https://doi.org/10.1007/s004420050613
Kovacs K, Ranson KJ, Kharuk VI (2005) Detecting siberian silk moth damage in central Siberia using multi-temporal MODIS data. In: International workshop of the analysis of multi-temporal remote sensing images, pp 25–29. https://doi.org/10.1109/AMTRSI.2005.1469833
Kress A, Saurer M, Büntgen U et al (2009) Summer temperature dependency of larch budmoth outbreaks revealed by Alpine tree-ring isotope chronologies. Oecologia 160:353–365. https://doi.org/10.1007/s00442-009-1290-4
Kulman HM (1971) Effects of insect defoliation on growth and mortality of trees. Ann Rev Entomol 16:289–324. https://doi.org/10.1146/annurev.en.16.010171.001445
Kyle CH, Liu J, Gallagher ME et al (2020) Stochasticity and infectious disease dynamics: density and weather effects on a fungal insect pathogen. Am Nat 195(3):504–523. https://doi.org/10.1086/707138
Lait LA, Hebert PDN (2018) Phylogeographic structure in three North American tent caterpillar species (Lepidoptera: Lasiocampidae): Malacosoma americana, M. californica, and M. disstria. Peerj 6:e4479. https://doi.org/10.7717/peerj.4479
Lance DR, Elkinton JS, Schwalbe CP (1987) Behavior of late-instar gypsy moth larvae in high and low density populations. Ecol Entomol 12(3):267–273. https://doi.org/10.1111/j.1365-2311.1987.tb01005.x
Larsson S, Ekbom B, Björkman C (2000) Influence of plant quality on pine sawfly population dynamics. Oikos 89(3):440–450. https://doi.org/10.1034/j.1600-0706.2000.890303.x
Lee K-S, Kang TH, Jeong JW et al (2015) Taxonomic review of the genus Lymantria (Lepidoptera: Erebidae: Lymantriinae) in Korea. Entomol Res 45(5):225–234. https://doi.org/10.1111/1748-5967.12116
Legault S, James PMA (2018) Parasitism rates of spruce budworm larvae: testing the enemy hypothesis along a gradient of forest diversity measured at different spatial scales. Environ Entomol 47(5):1083–1095. https://doi.org/10.1093/ee/nvy113
Legault S, Hébert C, Blais J et al (2012) Seasonal ecology and thermal constraints of Telenomus spp. (Hymenoptera: Scelionidae), egg parasitoids of the Hemlock looper (Lepidoptera: Geometridae). Environ Entomol 41(6):1290–1301. https://doi.org/10.1603/EN12129
Li L, Huanwen M, Xu S (2002) Bionomics of Dendrolimus superans Butler. J Inner Mongolia Agri Univ (Natural Science Edition) 23(1):101‒103.
Li S, Daudin JJ, Piou D et al (2015) Periodicity and synchrony of pine processionary moth outbreaks in France. Forest Ecol Manag 354:309–317. https://doi.org/10.1016/j.foreco.2015.05.023
Liebhold A, Kamata N (2000) Population dynamics of forest-defoliating insects. Popul Ecol 42(3):205–209. https://doi.org/10.1007/PL00011999
Liebhold A, Koenig WD, Bjørnstad ON (2004) Spatial synchrony in population dynamics. Ann Rev Ecol Evol Syst 35:467–490. https://www.jstor.org/stable/30034124
Liebhold AM, Halverson JA, Elmes GA (1992) Gypsy moth invasion in North America: a quantitative analysis. J Biogeogr 19(5):513–520. https://doi.org/10.2307/2845770
Liebhold AM, Gottschalk KW, Muzika R-M et al (1995) Suitability of North American tree species to the gypsy moth: a summary of field and laboratory tests. USDA GTR NE-211. https://doi.org/10.2737/NE-GTR-211. Accessed 21 October 2022
Liebhold AM, Sharov AA, Tobin PC (2007) Population biology of gypsy moth spread. In: Tobin PC, Blackburn LM (eds) “Slow the spread: a national program to manage the gypsy moth”. USDA GTR NRS-6:15–32. https://doi.org/10.2737/NRS-GTR-6. Accessed 21 October 2022
Liebhold AM, Plymale R, Elkinton JS et al (2013) Emergent fungal entomopathogen does not alter density dependence in a viral competitor. Ecology 94(6):1217–1222. https://doi.org/10.1890/12-1329.1
Liebhold AM, Berec L, Brockerhoff EG et al (2016) Eradication of invading insect populations: from concepts to applications. Ann Rev Entomol 61:335–352. https://doi.org/10.1146/annurev-ento-010715-023809
Liebhold AM, Björkman C, Roques A et al (2020) Outbreaking forest insect drives phase synchrony among sympatric folivores: Exploring potential mechanisms. Popul Ecol 62(4):372–384. https://doi.org/10.1002/1438-390X.12060
Liebhold AM, Hajek AE, Walter JA et al (2022) Historical change in the outbreak dynamics of an invading forest insect. Biol Invasions 24:879–889. https://doi.org/10.1007/s10530-021-02682-6
Lumley LM, Pouliot E, Laroche J et al (2020) Continent-wide population genomic structure and phylogeography of North America’s most destructive conifer defoliator, the spruce budworm (Choristoneura fumiferana). Ecol Evol 10(2):914–927. https://doi.org/10.1002/ece3.5950
Lyytikäinen-Saarenmaa P, Varama M, Anderbrant O et al (2001) Predicting pine sawfly population densities and subsequent defoliation with pheromone traps. In: Integrated management and dynamics of forest defoliating insects, Proceedings, USDA GTR NE-277:108–116. https://www.fs.usda.gov/nrs/pubs/gtr/gtr_ne277.pdf. Accessed 21 October 2022
Maclauchlan LE, Brooks JE, Hodge JC (2006) Analysis of historic western spruce budworm defoliation in south central British Columbia. For Ecol Manag 226(1–3):351–356. https://doi.org/10.1016/j.foreco.2006.02.003
MacLean DA (2016) Impacts of insect outbreaks on tree mortality, productivity, and stand development. Can Entomol 148(Suppl 1):138–159. https://doi.org/10.4039/tce.2015.24
MacLean DA, Ebert P (1999) The impact of hemlock looper (Lambdina fiscellaria fiscellaria (Guen.)) on balsam fir and spruce in New Brunswick, Canada. Forest Ecol Manag 120(103):77–87. https://doi.org/10.1016/S0378-1127(98)00527-1
MacLean DA, Amirault P, Amos-Binks L et al (2019) Positive results of an early intervention strategy to suppress a spruce budworm outbreak after five years of trials. Forests 10(5):448. https://doi.org/10.3390/f10050448
MacPhee A, Newton A, McRae KB (1988) Population studies on the winter moth Operophtera brumata (L) (Lepidoptera: Geometridae) in apple orchards in Nova Scotia. Can Entomol 120(1):73–83. https://doi.org/10.4039/Ent12073-1
Maeto K (1991) Outbreaks of Dendrolimus superans (Butler) (Lepidoptera: Lasiocampidae) related to weather in Hokkaido. App Entomol Zool 26(2):275–277. https://doi.org/10.1303/aez.26.275
Maksimov SA (1999) On factors responsible for population outbreaks in nun moth (Lymantria monacha L.). Russian J Ecol 30:47–51
Malakar R, Elkinton JS, Hajek AE et al (1999) Within-host interactions of Lymantria dispar (Lepidoptera: Lymantriidae) nucleopolyhedrosis virus and Entomophaga maimaiga (Zygomycetes: Entomophthorales). J Invertebr Pathol 73(1):91–100. https://doi.org/10.1006/jipa.1998.4806
Malakar RD (1997) Interactions between two gypsy moth (Lymantria dispar L.) pathogens: nuclear polyhedrosis virus and Entomophaga maimaiga (Entomophthorales: Zygomycetes). UMASS, PhD Dissertation. https://scholarworks.umass.edu/dissertations/AAI9809364/. Accessed 21 October 2022
Mamet SD, Chun KP, Metsaranta JM et al (2015) Tree rings provide early warning signals of jack pine mortality across a moisture gradient in the southern boreal forest. Environ Res Lett 10(8):084021. https://doi.org/10.1088/1748-9326/10/8/084021
Mannai Y, Ben Jamâa ML, M’nara S et al (2010) Biology of Tortrix viridana (Lep., Tortricidae) in cork oak forests of North-West Tunisia 57:153–160. https://www.iobc-wprs.org/members/shop_en.cfm
Marques JF, Wang HL, Svensson GP et al (2014) Genetic divergence and evidence for sympatric host-races in the highly polyphagous brown tail moth, Euproctis chrysorrhoea (Lepidoptera: Erebidae). Evol Ecol 28:829–848. https://doi.org/10.1007/s10682-014-9701-3
Martin JC, Mesmin X, Buradino M et al (2022) Complex drivers of phenology in the pine processionary moth: lessons from the past. Agric for Entomol 24(2):247–259. https://doi.org/10.1111/afe.12488
Martinat PJ, Allen DC (1987) Relationship between outbreaks of saddled prominent, Heterocampa guttivitta (Lepidoptera: Notodontidae), and drought. Environ Entomol 16(1):246–249. https://doi.org/10.1093/ee/16.1.246
Mason CJ, McManus ML (1981) Larval dispersal of the gypsy moth. In: Doane CC, McManus ML (eds) The Gypsy moth: research toward integrated pest management. USDA APHIS TB-1584:161–202. https://handle.nal.usda.gov/10113/CAT82474520. Accessed 24 October 2022
Mason RR (1976) Life tables for a declining population of Douglas-fir tussock moth in northeastern Oregon. Ann Entomol Soc Am 69(1):948–958. https://doi.org/10.1093/aesa/69.5.948
Mason RR (1978) Synchronous patterns in an outbreak of Douglas-fir tussock moth. Environ Entomol 7(5):672–675. https://doi.org/10.1093/ee/7.5.672
Mason RR (1996) Dynamic behavior of Douglas-fir tussock moth populations in the Pacific Northwest. For Sci 42(2):182–191. https://academic.oup.com/forestscience/article/42/2/182/4627302. Accessed 24 October 2022
Mason RR, Torgersen TR (1987) Dynamics of a nonoutbreak population of the Douglas-fir tussock moth (Lepidoptera, Lymantriidae) in southern Oregon. Environ Entomol 16(6):1217–1227. https://doi.org/10.1093/ee/16.6.1217
Mason RR, Torgersen TR, Wickman B et al (1983) Natural regulation of a Douglas-fir tussock moth (Lepidoptera, Lymantriidae) population in the Sierra-Nevada. Environ Entomol 12(2):587–594. https://doi.org/10.1093/ee/12.2.587
Mason RR, Scott DW, Paul HG (1993) Forecasting outbreaks of the Douglas-fir tussock moth from lower crown cocoon samples. USDA PNW-RP-460:1–12. https://doi.org/10.2737/PNW-RP-460
May RM (1975) Deterministic models with chaotic dynamics. Nature 256:165–166. https://doi.org/10.1038/256165a0
Mayfield AE III, Allen DC, Briggs RD (2007) Site and stand conditions associated with pine false webworm populations and damage in mature eastern white pine plantations. North J Appl for 24(3):168–176. https://doi.org/10.1093/njaf/24.3.168
McCullough DG (2000) A review of factors affecting the population dynamics of jack pine budworm (Choristoneura pinus pinus Freeman). Popul Ecol 42(3):243–256. https://doi.org/10.1007/PL00012003
McKnight ME (1974) Parasitoids of western spruce budworm in Colorado. Environ Entomol 3(1):186–187. https://doi.org/10.1093/ee/3.1.186
Meigs GW, Kennedy RE, Gray AN et al (2015) Spatiotemporal dynamics of recent mountain pine beetle and western spruce budworm outbreaks across the Pacific Northwest Region, USA. Forest Ecol Manag 339:71–86. https://doi.org/10.1016/j.foreco.2014.11.030
Melin M, Viiri H, Tikkanen OP et al (2020) From a rare inhabitant into a potential pest–status of the nun moth in Finland based on pheromone trapping. Silva Fennica 54(1):10262. https://doi.org/10.14214/sf.10262
Mirchev P, Georgiev G, Zaemdzhikova G et al (2021) Impact of egg parasitoids on pine processionary moth Thaumetopoea pityocampa (Denis & Schiffermüller, 1775) (Lepidoptera: Notodontidae) in a new habitat. Acta Zool Bulg 73(1):131–134. https://www.researchgate.net/publication/350484967
Mitter C, Futuyma D (1977) Parthenogenesis in Fall Cankerworm, Alsophila pometaria (Lepidoptera: Geometridae). Entomol Exp Appl 21(2):192–198. https://doi.org/10.1111/j.1570-7458.1977.tb02672.x
Mitter C, Neal JW, Gott KM et al (1987) A geographic comparison of pseudogamous populations of the fall cankerworm (Alsophila pometaria). Entomol Exp Appl 43(2):133–143. https://doi.org/10.1111/j.1570-7458.1987.tb03597.x
Moraal LG, Jagers op Akkerhuis GAJM (2011) Changing patterns in insect pests on trees in the Netherlands since 1946 in relation to human induced habitat changes and climate factors-An analysis of historical data. Forest Ecol Manag 261(1):50‒61.https://doi.org/10.1016/j.foreco.2010.09.024
Moran PAP (1953) The statistical analysis of the Canadian Lynx cycle. Australian J Zool 1(3):291–298. https://doi.org/10.1071/ZO9530291
Morin RS, Liebhold AM (2016) Invasive forest defoliator contributes to the impending downward trend of oak dominance in eastern North America. Forestry 89(3):284–289. https://doi.org/10.1093/forestry/cpv053
Morin RS, Liebhold AM, Luzader ER et al (2005) Mapping host-species abundance of three major exotic forest pests. USDA NE- 726:11. https://doi.org/10.2737/NE-RP-726
Moulinier J, Lorenzetti F, Bergeron Y (2013) Effects of a forest tent caterpillar outbreak on the dynamics of mixedwood boreal forests of eastern Canada. Écoscience 20(2):182–193. https://doi.org/10.2980/20-2-3588
Murdoch WW, Chesson J, Chesson PL (1985) Biological control in theory and practice. Am Nat 125(3):344–366. https://doi.org/10.1086/284347
Murray KM, Elkinton JS, Woods SA (1989) Epizootiology of gypsy moth nucleopolyhedrous virus. In: Wallner WE, McManus KA (tech coords) Proceedings, Lymantriidae: a comparison of features of New and Old World tussock moths. USDA NE-123:439–453. https://doi.org/10.2737/NE-GTR-123
Myers JH, Cory JS (2013) Population cycles in forest Lepidoptera revisited. In: Futuyma DJ (ed) The annual review of ecology, evolution, and eystematics 44:565–592. https://doi.org/10.1146/annurev-ecolsys-110512-135858
Nakajima H (1991) Two new species of the genus Operophtera (Lepidoptera, Geometridae) from Japan. Lep Sci 42(3): 195–205. https://doi.org/10.18984/lepid.42.3_195
Nakládal O, Brinkeová H (2015) Review of historical outbreaks of the nun moth (Lymantria monacha) with respect to host tree species. J For Sci 61(1):18–26. https://doi.org/10.17221/94/2014-JFS
Nealis V, Régnière J (2021) Ecology of outbreak populations of the western spruce budworm. Ecosphere 12(7):e03667. https://doi.org/10.1002/ecs2.3667
Nealis VG (1995) Population biology of the jack pine budworm. In: Volney WJA, Nealis VG, Howse GM et al (eds) Jack pine budworm biology and management. Proceedings of the jack pine budworm Symposium. Nat Res Can, Info Rep NOR-X-342:55–71. https://d1ied5g1xfgpx8.cloudfront.net/pdfs/12135.pdf. Accessed 24 October 2022
Nealis VG (2003) Host-plant relationships and comparative ecology of conifer-feeding budworms (Choristoneura spp.). In: McManus ML, Liebhold AM (eds) Proceedings ecology, survey and management of forest insects. USDA NE-311:68–71. https://www.iufro.org/download/file/4456/75/70307-krakow02.pdf#page=75
Nealis VG, Régnière J (2014) An individual-based phenology model for western spruce budworm (Lepidoptera: Tortricidae). Can Entomol 146(3):306–320. https://doi.org/10.4039/tce.2013.67
Nealis VG, Régnière J (2016) Why western spruce budworms travel so far for the winter. Ecol Entomol 41(5):633–641. https://doi.org/10.1111/een.12336
Nedorezov LV (2019) Identification of the type of population dynamics type of green oak tortrix with a generalized discrete logistic model. Bio Bull Rev 9:243–249. https://doi.org/10.1134/S2079086419030071
Negrón JF, Lynch AM, Schaupp WC Jr et al (2014) Douglas-fir tussock moth- and Douglas-fir beetle-caused mortality in a Ponderosa pine/Douglas-fir forest in the Colorado Front Range, USA. Forests 5(12):3131–3146. https://doi.org/10.3390/f5123131
Neilson MM, Morris RF (1964) Regulation of European spruce sawfly numbers in the Maritime Provinces of Canada from 1937 to 1963. Can Entomol 96(5):773–784. https://doi.org/10.4039/Ent96773-5
Nilssen AC, Tenow O, Bylund H (2007) Waves and synchrony in Epirrita autumnata/Operophtera brumata outbreaks. II. Sunspot activity cannot explain cyclic outbreaks. J Anim Ecol 76(2):269–275. https://doi.org/10.1111/j.1365-2656.2006.01205.x
Oswald WW, Doughty ED, Foster DR et al (2017) Evaluating the role of insects in the middle-Holocene Tsuga decline. J Torrey Bot Soc 144(1):35–39. https://harvardforest.fas.harvard.edu/publications/pdfs/Oswald_JTorrBot_2017.pdf
Parry D (1995) Larval and pupal parasitism of the forest tent caterpillar, Malacosoma disstria Hübner (Lepidoptera: Lasiocampidae), in Alberta, Canada. Can Entomol 127(6):877‒893.https://doi.org/10.4039/Ent127877-6
Parry D, Spence JR, Volney WJA (1997) Responses of natural enemies to experimentally increased populations of the forest tent caterpillar, Malacosoma disstria. Ecol Entomol 22(1):97‒108.https://doi.org/10.1046/j.1365-2311.1997.00022.x
Parry D, Goyer RA, Lenhard GJ (2001) Macrogeographic clines in fecundity, reproductive allocation, and offspring size of the forest tent caterpillar Malacosoma disstria. Ecol Entomol 26(3):281–291. https://doi.org/10.1046/j.1365-2311.2001.00319.x
Parry D, Herms DA, Mattson WJ (2003) Responses of an insect folivore and its parasitoids to multiyear experimental defoliation of aspen. Ecology 84(7):1768–1783. https://doi.org/10.1890/0012-9658(2003)084[1768:ROAIFA]2.0.CO;2
Pasquarella VJ, Elkinton JS, Bradley BA (2018) Extensive gypsy moth defoliation in southern New England characterized using Landsat satellite observations. Biol Invasions 20:3047–3053. https://doi.org/10.1007/s10530-018-1778-0
Pelletier G, Piché C (2003) Species of Telenomus (Hymenoptera: Scelionidae) associated with the hemlock looper (Lepidoptera: Geometridae) in Canada. Can Entomol 135(1):23–39. https://doi.org/10.4039/n02-035
Peltonen M, Liebhold AM, Bjørnstad ON et al (2002) Spatial synchrony in forest insect outbreaks: roles of regional stochasticity and dispersal. Ecology 83(11):3120–3129. https://doi.org/10.1890/0012-9658(2002)083[3120:SSIFIO]2.0.CO;2
Pepi AA, Broadley HJ, Elkinton JS (2016) Density-dependent effects of larval dispersal mediated by host plant quality on populations of an invasive insect. Oecologia 182: 499–509. Erratum Oecologia 185(2017):533–535. https://doi.org/10.1007/s00442-016-3689-z
Pérez-Contreras T, Soler JJ, Soler M (2003) Why do pine processionary caterpillars Thaumetopoea pityocampa (Lepidoptera, Thaumetopoeidae) live in large groups? An experimental study. Ann Zool Fenn 40(6):505–515. https://www.jstor.org/stable/23736507. Accessed 25 October 2022
Pimentel CS, Ferreira C, Santos M et al (2017) Spatial patterns at host and forest stand scale and population regulation of the pine processionary moth Thaumetopoea pityocampa. Agri for Entomol 19(2):200–209. https://doi.org/10.1111/afe.12201
Piper FI, Gundale MJ, Fajardo A (2015) Extreme defoliation reduces tree growth but not C and N storage in a winter-deciduous species. Ann Bot 115(7):1093–1103. https://doi.org/10.1093/aob/mcv038
Płatek K (2007) Variability of population density of the nun moth (Lymantria monacha L.) larvae in the Tuczno Forest District in the years 1996–2003. Sylwan 151(9):57–65. https://doi.org/10.26202/sylwan.2006112
Plenzich C, Despland E (2018) Host-plant mediated effects on group cohesion and mobility in a nomadic gregarious caterpillar. Behav Ecol Sociobiol 72:7p. https://doi.org/10.1007/s00265-018-2482-x
Pogue MG, Schaefer PW (2007) A review of selected species of Lymantria Hübner [1819] (Lepidoptera: Noctuidae: Lymantriinae) from subtropical and temperate regions of Asia, including the descriptions of three new species, some potentially invasive to North America. USDA FHTET 2006–07. https://handle.nal.usda.gov/10113/45484
Pschorn-Walcher H (1987) Interspecific competition between the principal larval parasitoids of the pine sawfly, Neodiprion sertifer (Geoff.) (Hym.: Diprionidae). Oecologia 73:621–625. https://doi.org/10.1007/BF00379426
Pureswaran DS, Johns R, Heard SB et al (2016) Paradigms in eastern spruce budworm (Lepidoptera: Tortricidae) population ecology: a century of debate. Environ Entomol 45(6):1333–1342. https://doi.org/10.1093/ee/nvw103
Pureswaran DS, Neau M, Marchand M et al (2019) Phenological synchrony between eastern spruce budworm and its host trees increases with warmer temperatures in the boreal forest. Ecol Evol 9(1):576–586. https://doi.org/10.1002/ece3.4779
Purrini K (1979) On natural diseases of Euproctis chrysorrhoea L (Lep., Lymantriidae) in Bavaria, 1977. Anz Schadlingskd Pfl 52:56–58. https://doi.org/10.1007/BF01988653
Quezada-Garcia R, Fuentealba A, Nguyen N et al (2015) Do offspring of insects feeding on defoliation-resistant trees have better biological performance when exposed to nutritionally-imbalanced food? InSects 6(1):112–121. https://doi.org/10.3390/insects6010112
Radeloff VC, Mladenoff DJ, Boyce MS (2000) The changing relation of landscape patterns and jack pine budworm populations during an outbreak. Oikos 90(3):417–430. https://doi.org/10.1034/j.1600-0706.2000.900301.x
Rahimzadeh-Bajgiran P, Weiskittel A, Kneeshaw D et al (2018) Detection of annual spruce budworm defoliation and severity classification using Landsat imagery. Forests 9(6):357. https://doi.org/10.3390/f9060357
Raymond B, Hails RS (2007) Variation in plant resource quality and the transmission and fitness of the winter moth, Operophtera brumata nucleopolyhedrovirus. Biol Control 41(2):237‒245.https://doi.org/10.1016/j.biocontrol.2007.02.005
Raymond B, Vanbergen A, Pearce I et al (2002) Host plant species can influence the fitness of herbivore pathogens: the winter moth and its nucleopolyhedrovirus. Oecologia 131:533–541. https://doi.org/10.1007/s00442-002-0926-4
Reardon RC (1976) Parasite incidence and ecological relationships in field populations of gypsy moth larvae and pupae. Environ Entomol 5(5):981–987. https://doi.org/10.1093/ee/5.5.981
Régnière J, Lysyk TJ (1995) Population dynamics of the spruce budworm, Choristoneura fumiferana. In: Armstrong JA, Ives WGH (eds) Forest insect pests in Canada. NRCAN, CFS/LFC, Science and Sustainable Dev’t Directorate, Ottawa, ON, pp 95–105. https://cfs.nrcan.gc.ca/publications?id=17004. Accessed 25 October 2022
Régnière J, Nealis VG (2018) Two sides of a coin: host-plant synchrony fitness trade-offs in the population dynamics of the western spruce budworm. Insect Science 25(1):117–126. https://doi.org/10.1111/1744-7917.12407
Régnière J, Nealis VG (2019) Density dependence of egg recruitment and moth dispersal in spruce budworms. Forests 10(8):706. https://doi.org/10.3390/f10080706
Régnière J, Delisle J, Pureswaran DS et al (2013) Mate-finding allee effect in spruce budworm population dynamics. Entomol Exp Appl 146(1):112–122. https://doi.org/10.1111/eea.12019
Régnière J, Cooke BJ, Béchard A et al (2019a) Dynamics and management of rising outbreak spruce budworm populations. Forests 10(9):748. https://doi.org/10.3390/f10090748
Régnière J, Delisle J, Dupont A et al (2019b) The impact of moth migration on apparent fecundity overwhelms mating disruption as a method to manage spruce budworm populations. Forests 10(9):775. https://doi.org/10.3390/f10090775
Régnière J, Venier L, Welsh D (2021) Avian predation in a declining outbreak population of the spruce budworm, Choristoneura fumiferana (Lepidoptera: Tortricidae). InSects 12(8):720. https://doi.org/10.3390/insects12080720
Reilly JR, Hajek AE, Liebhold AM et al (2014) Impact of Entomophaga maimaiga (Entomophthorales: Entomophthoraceae) on outbreak gypsy moth populations (Lepidoptera: Erebidae): the role of weather. Environ Entomol 43(3):632–641. https://doi.org/10.1603/EN13194
Rhainds M, Kettela EG, Silk PJ (2012) Thirty-five years of pheromone-based mating disruption studies with Choristoneura fumiferana (Clemens) (Lepidoptera: Tortricidae). Can Entomol 144(3):379–395. https://doi.org/10.4039/tce.2012.18
Rhainds M, Lavigne D, Boulanger Y et al (2022) I know it when I see it: Incidence, timing and intensity of immigration in spruce budworm. Agric for Entomol 24(2):152–166. https://doi.org/10.1111/afe.12479
Robert LE, Sturtevant BR, Kneeshaw D et al (2020) Forest landscape structure influences the cyclic-eruptive spatial dynamics of forest tent caterpillar outbreaks. Ecosphere 11(8):e03096. https://doi.org/10.1002/ecs2.3096
Robson JRM, Conciatori F, Tardif JC et al (2015) Tree-ring response of jack pine and scots pine to budworm defoliation in central Canada. Forest Ecol Manag 347:83–95. https://doi.org/10.1016/j.foreco.2015.03.018
Rochefort S, Berthiaume R, Hébert C et al (2011) Effect of temperature and host tree on cold hardiness of hemlock looper eggs along a latitudinal gradient. J Insect Physiol 57(6):751–759. https://doi.org/10.1016/j.jinsphys.2011.02.013
Roelofs WL, Hill AS, Linn CE et al (1982) Sex pheromone of the winter moth, a geometrid with unusually low temperature precopulatory responses. Science 217(4560):657–659. https://doi.org/10.1126/science.217.4560.657
Roland J (1986) Parasitism of winter moth in British Columbia during build-up of its parasitoid Cyzenis albicans: Attack rate on oak v. apple. J Anim Ecol 55(1):215–234. https://doi.org/10.2307/4703
Roland J (1990a) Parasitoid aggregation: chemical ecology and population dynamics. In: Mackauer M, Ehler LE (eds) Critical issues in biological control. Intercept, Andover, pp 185–211
Roland J (1990b) Interaction of parasitism and predation in the decline of winter moth in Canada. In: Watt A, Leather SR, Hunter AF (eds) Population dynamics of forest insects, Chapter 26. Intercept Ltd, Andover, Hampshire, UK, pp 289–301. https://www.academia.edu/60341405/Population_Dynamics_of_forest_insects. Accessed 25 October 2022
Roland J (1994) After the decline: what maintains low winter moth density after successful biological control? J Anim Ecol 63(2):392–398. https://doi.org/10.2307/5556
Roland J (1995) Response to Bonsall & Hassell ‘Identifying density-dependent processes: a comment on the regulation of winter moth.’ J Anim Ecol 64(6):785–786. https://doi.org/10.2307/5859
Roland J, Embree DG (1995) Biological control of the winter moth. Ann Rev Entomol 40:475–492. https://doi.org/10.1146/annurev.en.40.010195.002355
Roland J, Denford KE, Jimenez L (1995) Borneol as an attractant for Cyzenis albicans, a tachinid parasitoid of the winter moth, Operophtera brumata L (Lepidoptera: Geometridae). Can Entomol 127(3):413–421. https://doi.org/10.4039/Ent127413-3
Ronnås C, Larsson S, Pitacco A et al (2010) Effects of colony size on larval performance in a processionary moth. Ecol Entomol 35(4):436–445. https://doi.org/10.1111/j.1365-2311.2010.01199.x
Rothman LD, Roland J (1998) Forest fragmentation and colony performance of forest tent caterpillar. Ecography 21(4):383–391. https://doi.org/10.1111/j.1600-0587.1998.tb00403.x
Royama T (1984) Population dynamics of the spruce budworm Choristoneura fumiferana. Ecol Monogr 54(4):429–462. https://doi.org/10.2307/1942595
Royama T, Eveleigh ES, Morin JRB et al (2017) Mechanisms underlying spruce budworm outbreak processes as elucidated by a 14-year study in New Brunswick, Canada. Ecol Monogr 87(4):600‒631.https://doi.org/10.1002/ecm.1270
Rozenberg P, Pâques L, Huard F et al (2020) Direct and indirect analysis of the elevational shift of larch budmoth outbreaks along an elevation gradient. Front Glob Chang 3:86. https://doi.org/10.3389/ffgc.2020.00086
Ruohomäki K, Haukioja E (1992) Interpopulation differences in pupal size and fecundity are not associated with occurrence of outbreaks in Epirrita autumnata (Lepidoptera, Geometridae). Ecol Entomol 17(1):69–75. https://doi.org/10.1111/j.1365-2311.1992.tb01041.x
Ruohomäki K, Tanhuanpää M, Ayres MP et al (2000) Causes of cyclicity of Epirrita autumnata (Lepidoptera, Geometridae): grandiose theory and tedious practice. Popul Ecol 42(3):211–223. https://doi.org/10.1007/PL00012000
Ruuhola T, Salminen J-P, Haviola S et al (2007) Immunological memory of mountain birches: effects of phenolics on performance of the autumnal moth depend on herbivory history of trees. J Chem Ecol 33:1160–1176. https://doi.org/10.1007/s10886-007-9308-z
Ruuhola T, Yang S, Ossipov V et al (2008) Foliar oxidases as mediators of the rapidly induced resistance of mountain birch against Epirrita autumnata. Oecologia 154:725–730. https://doi.org/10.1007/s00442-007-0869-x
Ryall KL (2010) Effects of larval host plant species on fecundity of the generalist insect herbivore Ennomos subsignarius (Lepidoptera: Geometridae). Environ Entomol 39(1):121–126. https://doi.org/10.1603/EN09117
Ryan RB (1983) Population-density and dynamics of larch casebearer (Lepidoptera: Coleophoridae) in the Blue Mountains of Oregon and Washington before the build-up of exotic parasites. Can Entomol 115(9):1095–1102. https://doi.org/10.4039/Ent1151095-9
Ryan RB (1986) Analysis of life-tables for the larch casebearer (Lepidoptera, Coleophoridae) in Oregon. Can Entomol 118(12):1255–1263. https://doi.org/10.4039/Ent1181255-12
Ryan RB (1997) Before and after evaluation of biological control of the larch casebearer (Lepidoptera: Coleophoridae) in the Blue Mountains of Oregon and Washington, 1972–1995. Environ Entomol 26(3):703–715. https://doi.org/10.1093/ee/26.3.703
Sabbahi R, Royer L, O’Hara JE et al (2018) A review of known parasitoids of hemlock looper (Lepidoptera: Geometridae) in Canada and first records of egg and larval parasitoids in Labrador forests. Can Entomol 150(4):499–510. https://doi.org/10.4039/tce.2018.27
Salis L, Lof M, van Asch M et al (2016) Modeling winter moth Operophtera brumata egg phenology: nonlinear effects of temperature and developmental stage on developmental rate. Oikos 125: 1772–1781. Erratum 2017 Oikos 126:1522. https://doi.org/10.1111/oik.03257; https://doi.org/10.1111/oik.04819
Salman MHR, Hellrigl K, Minerbi S et al (2016) Prolonged pupal diapause drives population dynamics of the pine processionary moth (Thaumetopoea pityocampa) in an outbreak expansion area. Forest Ecol Manag 361:375–381. https://doi.org/10.1016/j.foreco.2015.11.035
Salminen JP, Karonen M (2011) Chemical ecology of tannins and other phenolics: we need a change in approach. Funct Ecol 25(2):325–338. https://doi.org/10.1111/j.1365-2435.2010.01826.x
Santiago O (2022) Western spruce budworm outbreak associated with wet periods in the Colorado Front Range: a multicentury reconstruction (CSU Theses and Dissertations). https://mountainscholar.org/handle/10217/235662. Accessed 27 October 2022
Saulnier M, Roques A, Guibal F et al (2017) Spatiotemporal heterogeneity of larch budmoth outbreaks in the French Alps over the last 500 years. Can J Forest Res 47(5):667–680. https://doi.org/10.1139/cjfr-2016-0211
Schaefer PW (1986) Bibliography of the browntail moth, Euproctis chrysorrhoea (L) (Lepidoptera: Lymantriidae) and its natural enemies. Del Agr Exp Sta Bull: 1–66.
Schmitt T (2007) Molecular biogeography of Europe: pleistocene cycles and postglacial trends. Front Zool 4:11. https://doi.org/10.1186/1742-9994-4-11
Schneider JC (1980) The role of parthenogenesis and female aptery in microgeographic, ecological adaptation in the fall cankerworm, Alsophila pometaria Harris (Lepidoptera: Geometridae). Ecology 61(5):1082–1090. https://doi.org/10.2307/1936827
Schopf R (1989) Spruce needle compounds and the susceptibility of Norway spruce (Picea abies Karst.) to attacks by the european sawfly, Gilpinia hercyniae Htg (Hym., Diprionidae). J Appl Entomol 107(1–5):435–445. https://doi.org/10.1111/j.1439-0418.1989.tb00280.x
Schott T, Hagen SB, Ims RA et al (2010) Are population outbreaks in sub-arctic geometrids terminated by larval parasitoids? J Anim Ecol 79(3):701–708. https://doi.org/10.1111/j.1365-2656.2010.01673.x
Schott T, Kapari L, Hagen SB et al (2013) Predator release from invertebrate generalists does not explain geometrid moth (Lepidoptera: Geometridae) outbreaks at high altitudes. Can Entomol 145(2):184–192. https://doi.org/10.4039/tce.2012.109
Schowalter TD (2017) Biology and management of the forest tent caterpillar (Lepidoptera: Lasiocampidae). J Integr Pest Manage 8(1):24;1–10. https://doi.org/10.1093/jipm/pmx022
Schroeder H, Degen B (2012) Phylogeography of the green oak leaf roller, Tortrix viridana L. (Lepidoptera, Tortricidae). M D Gesell Allg Ange 18:401–404. https://www.researchgate.net/publication/292953371_Phylogeography_of_the_green_oak_leaf_roller_Tortrix_viridana_L_Lepidoptera_Tortricidae
Schroeder H, Orgel F, Fladung M (2015) Performance of the green oak leaf roller (Tortrix viridana L.) on leaves from resistant and susceptible oak genotypes. M D Gesell Allg Ange 20:265–269. https://www.openagrar.de/receive/openagrar_mods_00022329
Seehausen ML, Bauce E, Régnière J et al (2015) Short-term influence of partial cutting on hemlock looper (Lepidoptera: Geometridae) parasitism. Agric for Entomol 17(4):347–354. https://doi.org/10.1111/afe.12113
Seixas Arnaldo P, Oliveira I, Santos J et al (2011) Climate change and forest plagues: the case of the pine processionary moth in Northeastern Portugal. For Sys 20(3):508–515. https://doi.org/10.5424/fs/20112003-11394
Senf C, Campbell EM, Pflugmacher D et al (2017) A multi-scale analysis of western spruce budworm outbreak dynamics. Landscape Ecol 32:501–514. https://doi.org/10.1007/s10980-016-0460-0
Sharov AA, Liebhold AM (1998a) Bioeconomics of managing the spread of exotic pest species with barrier zones. Ecol Appl 8(3):833–845. https://doi.org/10.2307/2641270
Sharov AA, Liebhold AM (1998b) Model of slowing the spread of gypsy moth (Lepidoptera: Lymantriidae) with a barrier zone. Ecol Appl 8(4):1170–1179. https://doi.org/10.2307/2640970
Sharov AA, Roberts EA, Liebhold AM et al (1995) Gypsy moth (Lepidoptera: Lymantriidae) spread in the central Appalachians: three methods for species boundary estimation. Environ Entomol 24(6):1529–1538. https://doi.org/10.1093/ee/24.6.1529
Sharov AA, Liebhold AM, Roberts EA (1996) Spread of gypsy moth (Lepidoptera: Lymantriidae) in the central Appalachians: comparison of population boundaries obtained from male moth capture, egg mass counts, and defoliation records. Environ Entomol 25(4):783–792. https://doi.org/10.1093/ee/25.4.783
Sharov AA, Liebhold AM, Roberts EA (1997) Methods for monitoring the spread of gypsy moth (Lepidoptera: Lymantriidae) populations in the Appalachian mountains. J Econ Entomol 90(5):1259–1266. https://doi.org/10.1093/jee/90.5.1259
Sharov AA, Liebhold AM, Roberts EA (1998) Optimizing the use of barrier zones to slow the spread of gypsy moth (Lepidoptera: Lymantriidae) in North America. J Econ Entomol 91(1):165–174. https://doi.org/10.1093/jee/91.1.165
Sharov AA, Leonard D, Liebhold AM et al (2002a) “Slow the spread”: a national program to contain the gypsy moth. J Forest 100(5):30–36. https://academic.oup.com/jof/article/100/5/30/4608639. Accessed 27 October 2022
Sharov AA, Leonard D, Liebhold AM et al (2002b) Evaluation of preventive treatments in low-density gypsy moth populations using pheromone traps. J Econ Entomol 95(6):1205–1215. https://doi.org/10.1603/0022-0493-95.6.1205
Shepherd RF, Bennett DD, Dale JW et al (1988) Evidence of synchronized cycles in outbreak patterns of Douglas-fir tussock moth, Orgyia pseudotsugata (McDunnough) (Lepidoptera: Lymantriidae). Mem Entomol Soc Can 120(S146):107–121. https://doi.org/10.4039/entm120146107-1
Shepherd RF, Gray TG, Harvey GT (1995) Geographical distribution of Choristoneura species (Lepidoptera: Tortricidae) feeding on Abies, Picea, and Pseudotsuga in western Canada and Alaska. Can Entomol 127(6):813–830. https://doi.org/10.4039/Ent127813-6
Shigesada N, Kawasaki K (1997) Biological invasions: theory and practice. Oxford University Press, UK
Simchuk AP, Ivashov AV, Companiytsev VA (1999) Genetic patterns as possible factors causing population cycles in oak leafroller moth, Tortrix viridana L. Forest Ecol Manag 113(1):35‒49.https://doi.org/10.1016/S0378-1127(98)00340-5
Simmons MJ, Lee TD, Ducey MJ et al (2014) Effects of invasive winter moth defoliation on tree radial growth in eastern Massachusetts, USA. InSects 5(2):301–318. https://doi.org/10.3390/insects5020301
Skellam JG (1951) Random dispersal in theoretical populations. Biometrika 38(1/2):196–218. https://doi.org/10.2307/2332328
Skuhravý V (1987) A review of research on the nun moth (Lymantria monacha L.) conducted with pheromone traps in Czechoslovakia, 1973–1984. Anz Schadlingskd Pfl 60:96–98. https://doi.org/10.1007/BF01906038
Smith CC (1958) A note on the association of fall cankerworm (Alsophila pometaria (Harr.)) with winter moth (Operophtera brumata (Linn.)) (Lepidoptera: Geometridae). Can Entomol 90(9):538–540. https://doi.org/10.4039/Ent90538-9
Smitley DR, Bauer LS, Hajek AE et al (1995) Introduction and establishment of Entomophaga maimaiga, a fungal pathogen of gypsy moth (Lepidoptera: Lymantriidae) in Michigan. Environ Entomol 24(6):1685–1695. https://doi.org/10.1093/ee/24.6.1685
Solla A, Milanović S, Gallardo A et al (2016) Genetic determination of tannins and herbivore resistance in Quercus ilex. Tree Genet Genomes 12:117. https://doi.org/10.1007/s11295-016-1069-9
Sonia S, Morin H, Krause C (2011) Long-term spruce budworm outbreak dynamics reconstructed from subfossil trees. J Quat Sci 26(7):734–738. https://doi.org/10.1002/jqs.1492
Spear RJ (2005) The great gypsy moth war: a history of the first campaign in Massachusetts to eradicate the gypsy moth, 1890–1901. University of Massachusetts Press. https://www.jstor.org/stable/j.ctt5vk7pz
Speare AT, Colley RH (1912) The artificial use of the brown-tail fungus in Massachusetts: with practical suggestions for private experiment, and a brief note on a fungous disease of the gypsy caterpillar. Wright & Potter Printing Company, Boston. https://tile.loc.gov/storage-services/public/gdcmassbookdig/artificialuseofb00mass/artificialuseofb00mass.pdf. Accessed 31 October 2022
Stastny M, Battisti A, Petrucco‐Toffolo E et al (2006) Host‐plant use in the range expansion of the pine processionary moth, Thaumetopoea pityocampa. Ecol Entomol 31(5):481‒490.https://doi.org/10.1111/j.1365-2311.2006.00807.x
Sterling PH, Speight MR (1989) Comparative mortalities of the brown-tail moth, Euproctis chrysorrhoea (L.) (Lepidoptera: Lymantriidae), in south-east England. Bot J Linn Soc 101(1):69–78. https://doi.org/10.1111/j.1095-8339.1989.tb00137.x
Stoakley JT (1985) Outbreaks of winter moth, Operophthera brumata L. (Lep, Geometridae) in young plantations of Sitka spruce in Scotland: insecticidal control and population assessment using the sex attractant pheromone. Z Angew Entomol 99(1–5):153–160. https://doi.org/10.1111/j.1439-0418.1985.tb01973.x
Sukovata L (2010) Prediction and control of the nun moth Lymantria monacha L. (Lepidoptera, Lymantriidae). Dissertations and Monographs 14:128. https://www.researchgate.net/publication/266970365_Prediction_and_control_of_the_nun_moth_Lymantria_monacha_L_Lepidoptera_Lymantriidae. Accessed 31 October 2022
Swetnam TW, Lynch AM (1989) A tree-ring reconstruction of western spruce budworm history in the southern Rocky Mountains. For Sci 35(4):962–986. https://www.ltrr.arizona.edu/~ellisqm/outgoing/dendroecology2014/readings/Swetnam%20and%20Lynch.1989.A%20tree-ring%20reconstruction.pdf. Accessed 31 October 2022
Swetnam TW, Lynch AM (1993) Multicentury, regional-scale patterns of western spruce budworm outbreaks. Ecol Mono 63(4):399–424. https://doi.org/10.2307/2937153
Swetnam TW, Wickman BE, Paul HG et al (1995) Historical patterns of western spruce budworm and Douglas-fir tussock moth outbreaks in the northern Blue Mountains, Oregon, since A.D. 1700. USDA PNW-RP-484:27. https://doi.org/10.2737/PNW-RP-484
Tamburini G, Marini L, Hellrigl K et al (2013) Effects of climate and density-dependent factors on population dynamics of the pine processionary moth in the Southern Alps. Clim Change 121:701–712. https://doi.org/10.1007/s10584-013-0966-2
Tammaru T, Kaitaniemi P, Ruohomäki K (1996) Realized fecundity in Epirrita autumnata (Lepidotera: Geometridae): relation to body size and consequences to population dynamics. Oikos 77(3):407–416. https://doi.org/10.2307/3545931
Tammaru T, Tanhuanpää M, Ruohomäki K et al (2001) Autumnal moth—why autumnal? Ecol Entomol 26(6):646–654. https://doi.org/10.1046/j.1365-2311.2001.00363.x
Tanhuanpää M, Ruohomäki K, Uusipaikka E (2001) High larval predation rate in non-outbreaking populations of a geometrid moth. Ecology 82(1):281–289. https://doi.org/10.1890/0012-9658(2001)082[0281:HLPRIN]2.0.CO;2
Taylor CM, Hastings A (2005) Allee effects in biological invasions. Ecol Lett 8(8):895–908. https://doi.org/10.1111/j.1461-0248.2005.00787.x
Tenow O, Nilssen A (1990) Egg cold hardiness and topoclimatic limitations to outbreaks of Epirrita autumnata in northern Fennoscandia. J Appl Ecol 27(2):723–734. https://doi.org/10.2307/2404314
Tenow O, Nilssen AC, Bylund H et al (2007) Waves and synchrony in Epirrita autumnata/Operophtera brumata outbreaks. I. Lagged synchrony: regionally, locally and among species. J Anim Ecol 76(2):258–268. https://www.jstor.org/stable/4539126. Accessed 31 October 2022
Tenow O, Nilssen AC, Bylund H et al (2013) Geometrid outbreak waves travel across Europe. J Anim Ecol 82(1):84–95. https://doi.org/10.1111/j.1365-2656.2012.02023.x
Ticehurst M, Allen DC (1973) Notes on biology of Telenomus coelodasidis (Hymenoptera: Scelionidae) and its relationship to saddled prominent, Heterocampa guttivitta (Lepidoptera: Notodontidae). Can Entomol 105(8):1133–1143. https://doi.org/10.4039/Ent1051133-8
Tobin PC (2007) Space-time patterns during the establishment of a nonindigenous species. Popul Ecol 49:257–263. https://doi.org/10.1007/s10144-007-0043-7
Tobin PC, Blackburn L (2007) Slow the Spread: a national program to manage the gypsy moth. USDA, Forest Service, Newtown Square, PA. NRS-GTR-6:109. https://doi.org/10.2737/NRS-GTR-6
Tobin PC, Whitmire SL, Johnson DM et al (2007) Invasion speed is affected by geographical variation in the strength of Allee effects. Ecol Lett 10(1):36–43. https://doi.org/10.1111/j.1461-0248.2006.00991.x
Tobin PC, Robinet C, Johnson DM et al (2009) The role of Allee effects in gypsy moth, Lymantria dispar (L.), invasions. Popul Ecol 51:373–384. https://doi.org/10.1007/s10144-009-0144-6
Tobin PC, Gray DR, Liebhold AM (2014) Supraoptimal temperatures influence the range dynamics of a non-native insect. Divers Distrib 20(7):813–823. https://doi.org/10.1111/ddi.12197
Torgersen TR, Ryan RB (1981) Field biology of Telenomus californicus Ashmead, an important egg parasite of Douglas-fir tussock moth. Ann Entomol Soc Am 74(2):185–186. https://doi.org/10.1093/aesa/74.2.185
Torgersen TR, Campbell RW (1982) Some effects of avian predators on the western spruce budworm Choristoneura occidentalis Freeman (Lepidoptera, Tortricidae) in north central Washington. Environ Entomol 11(2):429–431. https://doi.org/10.1093/ee/11.2.429
Troubridge JT, Fitzpatrick SM (1993) A revision of the North American Operophtera (Lepidoptera: Geometridae). Can Entomol 125(2):379–397. https://doi.org/10.4039/Ent125379-2
Trudeau M, Mauffette Y, Rochefort S et al (2010) Impact of host tree on forest tent caterpillar performance and offspring overwintering mortality. Environ Entomol 39(2):498–504. https://doi.org/10.1603/EN09139
Uelmen JA Jr, Lindroth RL, Tobin PC et al (2016) Effects of winter temperatures, spring degree-day accumulation, and insect population source on phenological synchrony between forest tent caterpillar and host trees. Forest Ecol Manag 362:241–250. https://doi.org/10.1016/j.foreco.2015.11.045
van Dis NE, van der Zee M, Hut RA et al (2021) Timing of increased temperature sensitivity coincides with nervous system development in winter moth embryos. J Exp Biol 224(17):jeb242554. https://doi.org/10.1242/jeb.242554
Van Dyck H (2012) Dispersal under global change-the case of the pine processionary moth and other insects. In: Clobert J, Baquette M, Benton TG et al (eds) Dispersal Ecology and Evolution. Oxford University Press, UK, pp 357–365. https://doi.org/10.1093/acprof:oso/9780199608898.003.0028
Vane E, Waring K, Polinko A (2017) The influence of western spruce budworm on fire in Spruce-Fir forests. Fire Ecol 13:16–33. https://doi.org/10.4996/fireecology.1301016
Vanhanen H, Veleli TO, Paivinen S et al (2007) Climate change and range shifts in two insect defoliators: gypsy moth and nun moth—a model study. Silva Fenn 41(4):621–638. https://doi.org/10.14214/sf.469
Varley GC, Gradwell GR (1960) Key factors in population studies. J Anim Ecol 29(2):399–401. https://doi.org/10.2307/2213
Varley GC, Gradwell GR (1963) Predatory insects as density dependent mortality factors. In: Moore JA (ed) Proceedings, XVI International Congress of Zoology 1:240, Washington, DC. https://catalog.hathitrust.org/api/volumes/oclc/2721561.html
Varley GC, Gradwell GR (1968) Population models for the winter moth. In: Southwood TRE (ed.) Insect abundance: symposia of the Royal Entomological Society of London 4:132–142.
Varley GC, Gradwell GR (1970) Recent advances in insect population dynamics. Ann Rev Entomol 15:1–24. https://doi.org/10.1146/annurev.en.15.010170.000245
Varley GC, Gradwell GR, Hassell MP (1973) Insect population ecology: an analytical approach. Blackwell Scientific, Oxford, England.
Venier LA, Holmes SB (2010) A review of the interaction between forest birds and eastern spruce budworm. Environ Rev 18:191–207. https://doi.org/10.1139/A10-009
Vindstad OPL, Schott T, Hagen SB et al (2013) How rapidly do invasive birch forest geometrids recruit larval parasitoids? Insights from comparison with a sympatric native geometrid. Biol Invasions 15:1573–1589. https://doi.org/10.1007/s10530-012-0393-8
Vindstad OPL, Jepsen JU, Molvig H et al (2022) A pioneering pest: the winter moth (Operphtera brumata) is expanding its outbreak range into low Arctic shrub tundra. Arct Sci 8(2):450–470. https://doi.org/10.1139/as-2021-0027
Visser ME, van Noordwijk AJ, Tinbergen JM et al (1998) Warmer springs lead to mistimed reproduction in great tits (Parus major). Proc R Soc Ser B Biol Sci 265(1408):1867–1870. https://doi.org/10.1098/rspb.1998.0514
Visser ME, Holleman LJM (2001) Warmer springs disrupt the synchrony of oak and winter moth phenology. Proc R Soc Ser B Biol Sci 268(1464):289–294. https://doi.org/10.1098/rspb.2000.1363
Volney WJA (1994) Multi-century regional western spruce budworm outbreak patterns. Trends Ecol Evol 9(2):43–45. https://doi.org/10.1016/0169-5347(94)90265-8
Volney WJA, McCullough DG (1994) Jack pine budworm population behaviour in northwestern Wisconsin. Can J Forest Res 24(3):502–510. https://doi.org/10.1139/x94-067
Wagner TL, Leonard DE (1979) Aspects of mating, oviposition, and flight in the satin moth, Leucoma salicis (Lepidoptera: Lymantriidae). Can Entomol 111(7):833–840. https://doi.org/10.4039/Ent111833-7
Wagner TL, Leonard DE (1980) Mortality factors of satin moth, Leucoma salicis [Lep.: Lymantriidae], in aspen forests in Maine. Entomophaga 25:7–16. https://doi.org/10.1007/BF02377517
Walter JA, Finch FT, Johnson DM (2016) Re-evaluating fall cankerworm management thresholds for urban and suburban forests. Agric for Entomol 18(2):145–150. https://doi.org/10.1111/afe.12147
War AR, Paulraj MG, Ahmad T et al (2012) Mechanisms of plant defense against insect herbivores. Plant Signaling Behav 7(10):1306–1320. https://doi.org/10.4161/psb.21663
Ward SF, Aukema BH (2019) Climatic synchrony and increased outbreaks in allopatric populations of an invasive defoliator. Biol Invasions 21:685–691. https://doi.org/10.1007/s10530-018-1879-9
Ward SF, Venette RC, Aukema BH (2019) Cold tolerance of the invasive larch casebearer and implications for invasion success. Agric for Entomol 21(1):88–98. https://doi.org/10.1111/afe.12311
Ward SF, Eidson EL, Kees AM et al (2020a) Allopatric populations of the invasive larch casebearer differ in cold tolerance and phenology. Ecol Entomol 45(1):56–66. https://doi.org/10.1111/een.12773
Ward SF, Aukema BH, Fei S et al (2020b) Warm temperatures increase population growth of a nonnative defoliator and inhibit demographic responses by parasitoids. Ecology 101(11):e03156. https://doi.org/10.1002/ecy.3156
Wargo PM (1977) Armillariella mellea and Agrilus bilineatus and mortality of defoliated oak trees. For Sci 23(4):485–492. https://academic.oup.com/forestscience/article-abstract/23/4/485/4675948?redirectedFrom=fulltext#no-access-message
Watt AD, McFarlane AM (1991) Winter moth on Sitka spruce: synchrony of egg hatch and budburst, and its effect on larval survival. Ecol Entomol 16(3):387–390. https://doi.org/10.1111/j.1365-2311.1991.tb00231.x
Weber BC (1977) Parasitoids of the introduced pine sawfly, Diprion similis (Hymenoptera: Diprionidae), in Minnesota. Can Entomol 109(3):359‒364.https://doi.org/10.4039/Ent109359-3
Weseloh RM (1985) Predation by Calosoma sycophanta L. (Coleoptera: Carabidae): evidence for a large impact on gypsy moth, Lymantria dispar L. (Lepidoptera: Lymantriidae), pupae. Can Entomol 117(9):1117–1126. https://doi.org/10.4039/Ent1171117-9
Wickman BE, Seidel KW, Star GL (1986) Natural regeneration 10 years after a Douglas-fir tussock moth outbreak in northeastern Oregon. USDA PNW-RP-370:1–15. https://doi.org/10.2737/PNW-RP-370
Wigley PJ (1976) The Epizooliology of a nuclear polyhedrosis virus disease of the winter moth Operophtera brumata L., at Wistmanns Wood, Dartmoor. PhD thesis. University of Oxford, Oxford, UK
Williams DT, Straw NA, Day KR (2003) Defoliation of Sitka spruce by the European spruce sawfly, Gilpinia hercyniae (Hartig): a retrospective analysis using the needle trace method. Agric for Entomol 5(3):235–245. https://doi.org/10.1046/j.1461-9563.2003.00183.x
Williams DW, Birdsey RA (2003) Historical patterns of spruce budworm defoliation and bark beetle outbreaks in North American conifer forests: an atlas and description of digital maps. USDA NE-GTR-308:1–33. https://doi.org/10.2737/NE-GTR-308
Williams DW, Liebhold AM (1995a) Forest defoliators and climatic change: potential changes in spatial distribution of outbreaks of western spruce budworm (Lepidoptera: Tortricidae) and gypsy moth (Lepidoptera: Lymantriidae). Environ Entomol 24(1):1–9. https://doi.org/10.1093/ee/24.1.1
Williams DW, Liebhold AM (1995b) Influence of weather on the synchrony of gypsy moth (Lepidoptera: Lymantriidae) outbreaks in New England. Environ Entomol 24(5):987–995. https://doi.org/10.1093/ee/24.5.987
Williams DW, Fuester RW, Metterhouse WW et al (1992) Incidence and ecological relationships of parasitism in larval populations of Lymantria dispar (Lepidoptera: Lymantriidae). Biol Control 2(1):35–43. https://doi.org/10.1016/1049-9644(92)90073-M
Wilson CM, Vendettuoli JF, Orwig DA et al (2016) Impact of an invasive insect and plant defense on a native forest defoliator. InSects 7(3):45. https://doi.org/10.3390/insects7030045
Wint W (1983) The role of alternative host-plant species in the life of a polyphagous moth, Operophtera brumata (Lepidoptera: Geometridae). J Anim Ecol 52(2):439–450. https://doi.org/10.2307/4564
Witrowski Z (1975) Environmental regulation of population size of oak leaf roller moth (Tortrix viridana L.) in Niepolomice Forest. B Acad Pol Sci Biol 23(8):513–519.
Wong HR (1972) Spread of the European spruce sawfly, Diprion hercyniae (Hymenoptera: Diprionidae), in Manitoba. Can Entomol 104(5):755‒756.https://doi.org/10.4039/Ent104755-5
Wood DM, Yanai RD, Allen DC et al (2009) Sugar maple decline after defoliation by forest tent caterpillar. J For 107(1):29–37. https://academic.oup.com/jof/article/107/1/29/4598872. Accessed 1 November 2022
Wood DM, Parry D, Yanai RD et al (2010) Forest fragmentation and duration of forest tent caterpillar (Malacosoma disstria Hübner) outbreaks in northern hardwood forests. Forest Ecol Manag 260(7):1193–1197. https://doi.org/10.1016/j.foreco.2010.07.011
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Elkinton, J., Roehrig, A. (2023). Foliage Feeders. In: D. Allison, J., Paine, T.D., Slippers, B., Wingfield, M.J. (eds) Forest Entomology and Pathology. Springer, Cham. https://doi.org/10.1007/978-3-031-11553-0_9
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