Next Article in Journal
Identification and Spread of the Ghost Silverfish (Ctenolepisma calvum) among Museums and Homes in Europe
Next Article in Special Issue
Effect of Entomopathogenic Fungi, Beauveria bassiana (Cordycipitaceae), on the Bark Beetle, Ips typographus (L.), under Field Conditions
Previous Article in Journal
Energy Consumption and Cold Hardiness of Diapausing Fall Webworm Pupae
Previous Article in Special Issue
Efficacy of Biopesticides in the Management of the Cotton Bollworm, Helicoverpa armigera (Noctuidae), under Field Conditions
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Lymantria dispar (L.) (Lepidoptera: Erebidae): Current Status of Biology, Ecology, and Management in Europe with Notes from North America

1
Laboratory of Agricultural Zoology and Entomology, Department of Crop Science, Agricultural University of Athens, 75 Iera Odos Str., 11855 Athens, Greece
2
Department of Crop and Forest Sciences, Agrotecnio Centre, Universitat de Lleida, Av Rovira Roure 191, 25198 Lleida, Spain
3
AIMPLAS, Plastics Technology Centre, València Parc Tecnològic, Gustave Eiffel 4, 46980 Paterna, Spain
4
Department of Agronomy, Biotechnical Faculty, University of Ljubljana, Jamnikarjeva 101, 1000 Ljubljana, Slovenia
5
Laboratory of Entomology and Agricultural Zoology, Department of Agriculture, Crop Production and Rural Environment, University of Thessaly, Phytokou Str., 38446 Nea Ionia, Greece
*
Authors to whom correspondence should be addressed.
Insects 2022, 13(9), 854; https://doi.org/10.3390/insects13090854
Submission received: 12 August 2022 / Revised: 14 September 2022 / Accepted: 15 September 2022 / Published: 19 September 2022

Abstract

:

Simple Summary

In the current review, we gathered and summarized the up-to-date information on the life cycle, distribution, outbreaks, control, and health issues to humans and animals of the European Spongy moth. Overall, this noxious species is easily expanded to new areas, causing serious large-scale damage rapidly. The management of this insect is difficult since the chemicals are harmful to human health and the environment, and natural enemies are not able to cause sufficient reduction of the populations of L. dispar. Finally, the potential use of biotechnological and physical methods against L. dispar is discussed.

Abstract

The European Spongy moth, Lymantria dispar (L.) (Lepidoptera: Erebidae), is an abundant species found in oak woods in Central and Southern Europe, the Near East, and North Africa and is an important economic pest. It is a voracious eater and can completely defoliate entire trees; repeated severe defoliation can add to other stresses, such as weather extremes or human activities. Lymantria dispar is most destructive in its larval stage (caterpillars), stripping away foliage from a broad variety of trees (>500 species). Caterpillar infestation is an underestimated problem; medical literature reports that established populations of caterpillars may cause health problems to people and animals. Inflammatory reactions may occur in most individuals after exposure to setae, independent of previous exposure. Currently, chemical and mechanical methods, natural predators, and silvicultural practices are included for the control of this species. Various insecticides have been used for its control, often through aerial sprayings, which negatively affect biodiversity, frequently fail, and are inappropriate for urban/recreational areas. However, bioinsecticides based on various microorganisms (e.g., entomopathogenic viruses, bacteria, and fungi) as well as technologies such as mating disruption using sex pheromone traps have replaced insecticides for the management of L. dispar.

1. Introduction

Sporadic outbreaks of insect pests are a major challenge to forest health in many countries, leading to serious environmental resource losses and degradations. One of these pests is the spongy moth (formerly known as gypsy moth) Lymantria dispar (L.) (Lepidoptera: Erebidae), a notorious invasive polyphagous pest, causing widespread loss of leaves in forests in Europe, Asia, North America, and parts of Africa (Figure 1a) [1]. This species recently underwent a change to the common name since the word “gypsy” was considered to be an ethnic slur and now refers to the spongy egg masses [2]. It is also considered very harmful to orchards and urban environments [3,4,5]. In the species name of the L. dispar, “dispar” is derived from the Latin word that means “to separate”, depicting the conspicuous sexual dimorphism of this species [6]. Females are larger and more brightly coloured than males and do not fly even though they are winged [7]. The International Union for Conservation of Nature (IUCN) has categorized L. dispar as one of the 100 worst invaders globally [8]. According to the European and Mediterranean Plant Protection Organization [9], in the United States of America, L. dispar has been a quarantine pest since 1989, while in Europe it has been classified in the A1 list in Azerbaijan and Georgia since 2007 and 2018, respectively, and in the A2 list in Russia since 2014.
Lymantria dispar is a univoltine species with four distinct life stages: egg, larva (caterpillar), pupa, and adult (Figure 1b–f) [10,11]. More specifically, the front and vertex of the male’s head is pale gray to light brown; the antennae are bipectinates; and the shaft is completely scaled, with a light brown color and some fuscous scales apically. The forewing is 14.5–22 mm long [12] and is color brown. The hindwings are reddish-brown with a dark brown marginal band and light brown fringe [12]. The front and vertex of the female’s head is white, the scape is speckled white and brown, the antenna has short pectinations, the shaft and pectinations are fuscous, and the apex is white. The length of forewings in females is 20–30 mm [12], being the color white. The hindwing is white, has a discal spot faint, and has a V-shaped at end of the discal cell [12]. Egg clusters are teardrop shaped, their color is yellowish to brownish, are felt-like in appearance, and turn lighter in color with age. Normally, all individual eggs are hidden by the hairs of the female abdomen [12]. First instar larvae are about 3 mm long [6], are very light in weight, and their color is dark brown to black, while the later instar larvae are more colorful [13,14]. The final larval instar is sometimes up to 90 mm long [6]. Full-grown larvae are hairy and have on the dorsum two rows of blue tubercles on the first five segments and two rows of red tubercles on the following six segments [14]. Pupae are dark brown and teardrop shaped, without a silky cocoon. Female pupae are 15–35 mm long, while males are usually smaller than females with a length of about 15–20 mm [13].
The classification of L. dispar has been controversial in the past, but it is now generally accepted that the European spongy moth, Lymantria dispar dispar L., differs from the Asian spongy moth [15]. Indeed, apart from the European spongy moth, which is spread throughout Europe and can be found in all environmental zones, with the exception of the Alpine North and part of the Boreal zone [16], two other subspecies have been recognized: (i) L. dispar asiatica Vnukovskij, which is found mostly in China, in Korea, and in the east Ural Mountains, and (ii) L. dispar japonica Motschulsky, which occurs on the main islands of Japan [12]. However, all three subspecies are polyphagous [17,18], with L. dispar asiatica having a wider range of host plants than L. dispar dispar [15,19,20,21,22,23,24,25,26]. In addition, females of both Asian subspecies are capable of flight, in contrast to females of the European subspecies that are flightless [10,12,23,27,28], a fact that may impede the spread of the latter subspecies. However, females of the European subspecies have little to no selectivity during oviposition and they can deposit egg masses on available substrates than can be used as vehicles for the spread of this subspecies [29]. Similarly, females of L. dispar asiatica that are able to fly are more attracted to lights, especially at well-lit ports, where they lay eggs on ships, which greatly facilitates their dispersal [30,31]. Recently, several molecular tools based on the mitochondrial barcode region have been used for the identification of the three subspecies. It has been found that nucleotide substitutions within regions of mitogenomes of L. dispar may be a useful tool to distinguish among the subspecies and/or detect geographical origins [32].
Populations of L. dispar usually remain at low densities. However, under some circumstances that are not well understood, densities can increase rapidly and after few generations achieve pest status. It has been reported that the length of the non-outbreak periods may be linked to climate, being shorter in dry forests and longer in wet ones [33]. The projected increase in temperature will strongly affect the ecology and distribution of exothermic organisms and is likely to trigger outbreaks of certain insect pests [34]. Indeed, the increase in mean temperature is expected to have a positive effect on L. dispar dispersal in the more northern ecosystems. Moreover, apart from climate change, inadvertent transportation will help this species to colonize new northern European habitats, as has happened in North America [35].
Currently, management of L. dispar is mainly based on biopesticides [36,37]. Moreover, several biocontrol agents have been used for the control of L. dispar such as entomopathogenic microorganisms alone or in combinations [36,38,39,40,41,42,43,44,45,46,47,48]. Although parasitoids represent appropriate biological control agents [49], they have not been used very often in IPM programs for controlling L. dispar in Europe.
Due to a lack of review studies concerning L. dispar in Europe, we aimed to gather and present in detail the up-to-date information from the international bibliography, scientific databases, and journals on the following aspects: description of each life stage, lifespan, preferred plant species, distribution, damages and outbreaks, and various control and monitoring methods (i.e., traps, mating disruption, natural enemies, biological and chemical control). In addition to the considerable damage to forests, L. dispar larvae are an underestimated problem; established populations of larvae may cause health problems to people and animals. Thus, special emphasis will be given to the health problems and risks arising from the presence of L. dispar larvae in forests and urban/recreational areas for humans and the environment.

2. Biology

The lifespan of L. dispar adults is about a week, and male emergence usually takes place 1 or 2 days before the females [6]. Specifically, females die about one day after oviposition, whereas males survive for about a week, after mating with different females [11]. Lymantria dispar can mate and oviposit soon after adults emerge [10,12,50]. Moreover, females can attract males and mate within two hours of pupal eclosion [51,52]. The courtship behavior is very simple, a male approaches a female, and mating occurs only when the female lifts her wings to allow mating. Copulation lasts for up to an hour, but usually the passage of the spermatophore or sperm packet is accomplished in the first 10 min. After the termination of the sexual interaction, females begin to lay eggs [6,53,54]. Females mate once while males usually mate a few times [55]. Thus, since males are polygamous, almost all females are fertilized, even if males comprise only 17% of the total population [56]. The reproductiive timespan of females is shorter than a week. By the third day after the female’s emergence, their attractiveness decreases significantly, perhaps due to a depletion of the pheromone supply. Thus, there is little likelihood a female will mate if a mate has not been selected by then [6].
Mated females lay eggs on the tree trunks usually at less than 1 m from their pupation site because they are functionally flightless [12,23,27,28,57,58,59]. However, females that have not mated lay eggs that do not hatch and are usually scattered singly or in small, disorganized clusters [39]. Eggs are deposited in clutches directly on the bark or branches of host trees in late summer [12,60,61,62,63,64]. If a female is interrupted during the oviposition, she is able to initiate a new cluster [6]. In addition to host plants, eggs can be found on rocks or other immovable objects (e.g., firewood, recreational vehicles, Christmas trees, boat or cargo containers) and can overwinter there for eight to nine months [10,65]. Generally, females oviposit in the cooler or shady parts of the tree [12]. A female can lay from less than 100 to over 1000 eggs. Under optimal conditions, the mean number of eggs in a cluster is about 750, while at the end of an outbreak when the population begins to decline, it is about 300 [6]. For instance, in Spain, the mean number of eggs per cluster over the entire generation is 250–500 [57,58,59,66,67]. In addition, the egg clusters are covered with hair-like setae from the female’s abdomen to protect them for overwintering [44]. The hairs are long, straight, and generally conical at both ends [68]. Eggs can withstand temperatures below −30 °C (down to −31.7 °C), provided they are deposited in a protected area or insulated with snow [10]. The egg clusters are approximately 3.8 cm long and 1.9 cm wide, whereas the presence of smaller egg clusters indicates that the population of L. dispar is declining [69].
The first three weeks of the egg stage consist of embryonation followed by diapause, which is affected by cold and warm conditions [70]. A significant number of studies have been conducted on climatic factors that affect the three stages of diapause (i.e., pre-diapause, diapause, and post-diapause), revealing a complex, non-linear relationship between temperature and progress through the completion of diapause [6,71,72]. The development of the embryo is favored by higher temperatures, completing the prediapause phase in approximately 16 days at 25 °C, but at a lower temperature, this phase takes longer to complete (e.g., 48 d at 15 °C) [73]. This phase is characterized by high respiration rates and abundant morphological development of the embryo [60,73]. The well-developed embryo then enters the next phase, the diapause, as a fully differentiated pharate larva, which lasts several months [60,74], but the role of the temperature is crucial, since at low temperatures, diapause is terminated quickly [60,72,75,76,77]. This phase is characterized by low respiration and developmental rates favored by low temperatures [72]. After exposure to low temperatures to terminate the diapause, elevated temperatures affect the hatching, where at 25 °C, hatching is completed in 11–18 days, while at 15 °C, more time is needed (i.e., 14–25 days), and the respiration rates are again high during the postdiapause phase [78]. There is no evidence that the photoperiod can control diapause, but 60–150 days of low temperature exposure is required [77].
Egg hatching takes place in early spring to mid-May [10]. However, the temperature strongly affects the hatching and activity of new larvae. Most of them hatch within a week, while hatching of egg clusters deposited in cooler areas or at higher altitudes can extend up to a month [6]. Larvae overwinter as embryos protected in eggshells and emerge in spring [12]. Male larvae usually go through five instars, while females go through six instars [63]. However, it has been reported that larvae may go through as many as 11 instars before pupation [70]. If the newly hatched larvae emerge at temperatures lower than 7 °C, they remain on or near the egg cluster [6]. Heavy rainfall during egg hatch may result in drowning of larvae. Moreover, during rainy weather, the first-instar larvae may delay their migration and accumulate on the underside of leaves [79].
After hatching, the larvae feed on the foliage of the host plants for a period of six to eight weeks [10]. First instar larvae begin feeding by cutting small holes in the surface of leaves, whereas later instars feed on the edge of leaves [6]. A distinct change in the feeding rhythm of L. dispar occurs as the larvae develop and mature [80]. The larvae are positively phototropic and negatively geotropic when they leave the egg and spin a silk thread as they move [6]. In addition, phototropic changes shift their behavior, with early instar larvae strongly attracted to light and late-instar larvae indifferent or repelled by light [81]. Early instar larvae (typically first- to third-instar) feed on host leaves during the day and stay on the underside of foliage during the evening [61,82]. Late-instar larvae (fourth- to sixth-instar) feed on the canopy overnight, whereas at daybreak, they move downward in search of cryptic resting places (e.g., bark flaps or crevices, litter under the host tree) [52] as these sites provide protection from predators [83,84]. During the diurnal period of larval movement, it is very common for the late instar larvae to abandon the tree they were feeding on and move to a new one [85]. This is a mechanism that allows late instar larvae to use a wider range of plants than early instar larvae [86]. However, in elevated populations, such as populations of more than 1250 egg masses/ha, all larvae feed in the day and night and do not need to hide in a shelter [87]. Approximately 80% of defoliation is conducted by the fifth and sixth instar larvae [88]. In Central Europe, the larvae begin to feed in late April and continue for up to 10 weeks, until they pupate in late June–early July [89].
The larvae stop feeding just before the prepupal stage, which lasts only for about 2 days, where the larvae void the gut, surround themselves in a sparse silken net, and begin to contract in length. The prepupae remain relatively quiescent inside the silken net [6]. Pupation occurs in hidden places such as the underside of branches, cracks in bark, trunk crevices, and under stones or trunks on the soil [57,58,59]. The pupal stage lasts 7–14 days depending on climate and sex. Usually, males emerge a few days earlier than females [50,85].
Lymantria dispar adults do not feed, and although moisture is imbibed, their digestive system is not functional [6]. Τhe larvae are the most destructive life stage, as they can feed on a wide range of hosts [17,18,50,90,91,92,93]. In addition, voracious larvae can feed on host trees for up to 10 weeks [94]. The consumption of oak foliage by larvae is about 10 mg for each mg gain in larval biomass [95]. Each larva in a dense population is able to consume about 1270 mg of foliage (dry weight) and reach a weight of 114 mg. This is about 170 cm2 foliage corresponding to three red oak leaves. However, a large (750 mg) female larva typical of a sparse population could consume a total of 1000 cm2 of foliage [50]. Thus, the sixth instar female larvae are considered the most ravenous feeders and have often twice the size of full-grown male larvae [11].
Forest tree species can be categorized as “susceptible”, “resistant”, or “immune” to defoliation by L. dispar larvae [17,96]. “Susceptible” tree species are those that are consumed by all larval instars; “resistant” are the species that only some larval instars consume, or when susceptible species are not available (Table 1); and “immune” species are rarely, if ever, consumed by any larval instar. Some tree species are considered resistant to L. dispar larvae unless in close proximity to susceptible species. In the case that a preferred tree species is not available, the larvae may alternatively feed on the red and sugar maple, A. rubrum L. and A. saccharum Marshall (Sapindales: Sapindaceae); the American beech, Fagus grandifolia Ehrh. (Fagales: Fagaceae); and the American elm, Ulmus americana L. (Rosales: Ulmaceae) [10,17].
In Europe, the preferred hosts vary by region, but include species of Quercus, Carpinus, Alnus, Prunus, Populus, Gleditsia, Tilia, Corylus, and Robinia [63,97,98]. For instance, in Lithuania, which is at the northern limits of its range, species of birch (Betula) and alder (Alnus) are the primary hosts, while in Spain, Portugal, and Sardinia, the cork oak, Quercus suber L. (Fagales: Fagaceae), is the dominant host, and stands of this species have been frequently defoliated. The distribution of L. dispar in the rest of Europe is associated with the presence of up to seven species of Quercus, especially the Austrian oak, Q. cerris L.; the pedunculate oak, Q. robur L.; and the sessile oak, Q. petraea (Matt.) Liebl. (Fagales: Fagaceae), but this latter species is less preferred among the Central European oaks [98]. The hornbeam, Carpinus betulus L. (Fagales: Betulaceae), is usually mixed in stands of oaks in Central Europe and is considered an equally preferred host along with species of Populus, Alnus, and Salix [98,99]. In southern France and the Balkans, Q. suber, Q. pubescens, and Q. ilex serve as the main hosts. However, there is an exception to the close relationship between oak species and L. dispar populations in the Danube delta of Romania, where 27,000 ha of Populus and Salix stands serve as preferred hosts for L. dispar larvae [98].
In North America, L. dispar feed on >300 species of woody plants but prefer the species Quercus, Salix, Populus, and Betula [17]. More specifically, 148 host trees have been identified as highly susceptible hosts out of a total of 449 tree species that larvae can feed on [17]. Quercus and Salix are the most susceptible genera, with the remaining highly susceptible species coming from 28 other tree genera including Larix, a deciduous conifer [100]. In both Europe and North America, the variety of hosts plants the larvae utilize expands when they reach the fourth instar, including several conifers, such as some species of pine, spruce, and hemlock [101].
It has been reported that early instar larvae are not able to complete their development on non-deciduous conifers [18,102,103]. However, in outbreak mode, larvae will consume coniferous foliage, and these trees tend to be much less resistant to defoliation and may die after a single attack [104]. On the other hand, hardwood trees that are initially in good condition can produce new leaves after a L. dispar attack (which generally takes place in June and early July) and can often withstand several years of defoliation without dying [104]. Consequently, in the case of mixed pine–hardwood stands such as those of eastern North America, defoliation by larvae is largely limited to hardwood hosts, and outbreaks generally do not occur in stands in which the proportion of oaks or other susceptible host plant species is less than 20% of host basal area [105,106].
In Spain, L. dispar has been reported on Quercus sp., Castanea sp., Corylus sp., and Fagus sp. but also on Populus sp., Ulmus sp., Arbutus sp., Prunus sp., Acer sp., Salix sp., Betula sp., Alnus sp., or Pinus sp. It has been reported to damage the strawberry tree, Arbutus unedo L. 1753 (Ericales: Ericaceae), and coniferous species, such as the Aleppo pine; Pinus halepensis Mill., in the Balearic Islands and Catalonia; the maritime pine, Pinus pinaster Aiton, in central Spain and the Balearic Islands; and the radiata pine, Pinus radiata D.Don (Pinales: Pinaceae), in northern Spain [58,66]. This forms an important threat to public health as pine trees constitute a major species in urban/suburban environments and cover large forest areas in Southern Europe, while their presence is common in schools and other public areas, potentially affecting susceptible individuals, such as children.
It has been found in the provinces of Pontevedra (north-western Spain) and Asturias (northern Spain) in the outbreaks during 1952–1953 [107,108]. In northwestern Portugal, 290 ha of a 15-year-old plantation of P. radiata were severely defoliated in 1991 [109]. Moreover, Miller and Hanson [110], conducting laboratory tests, found that the first instar larvae originated from egg clusters collected in Oregon, USA, completed their development on different coniferous tree species including the white fir, Abies concolor (Gordon) Lindley ex Hildebrand; the blue spruce, Picea pungens Engelm.; the ponderosa pine, Pinus ponderosa Douglas ex C.Lawson; and the Douglas fir, Pseudotsuga menziesii (Mirbel) Franco (Pinales: Pinaceae). More recently, Castedo-Dorado et al. [111] reported that the L. dispar was able to complete development in the field and severely defoliated trees of P. radiata in Spain. Radiata pine is native to California, but has spread widely elsewhere, especially in the southern hemisphere, due to its planting for commercial forestry. In 1950, extensive planting of this species began in the Northern Iberian Peninsula [112]. Consequently, the presense of P. radiata in this region, along with other southern European countries, are the only areas where both radiata pine and L. dispar overlap, since radiata pine is absent from L. dispar’s invasion area in North America and the insect pest is absent in the southern hemisphere [111].

3. Ecology of L. dispar

3.1. Distribution

Lymantria dispar is a serious insect pest in southern and central Europe [34]. It was intentionally introduced to the east coast of North America from Western Europe in 1869 for silk production [12,50,52,113,114,115,116]. Professor L. Trouvelot maintained colonies of this species, attempting to reproduce better silkworm larvae by crossing them with the native silkworm, Antheraea polyphemus (Cramer) (Lepidoptera: Saturniidae), but a small number of L. dispar larvae escaped from his laboratory [98,115,117]. This species has been established there, reaching nearly the middle of the continent [118]; it has spread throughout New England and the adjoining provinces of Canada. The peak of the infestation has reached Maine, Wisconsin, Illinois, Indiana, Ohio, West Virginia, Virginia, North Carolina, Ontario, Quebec, New Brunswick, and Nova Scotia [27,119]. Lymantria dispar has become a much more serious pest in the United States than in its native regions [6,113,115,120,121,122]. Lymantria dispar has recently expanded to several ecosystems globally, where it was previously nonnative, due to high vehicle traffic, international shipping, and global warming, which favors its winter survival and enhances its feeding activity in northern regions, as shown both in research simulations and empirically [35].
Lymantria dispar is widely distributed in Europe, occurring in many environments of this continent, with the exception of Alpine North and partially the Boreal zone [9,16]. It is also found from latitude 60° N in mid-Scandinavia to 35° N on the Mediterranean coast and occurs from the Mediterranean scrub land to the temperate deciduous forests [118]. The northern limit proceeds through southern Sweden and Finland and descends from about 60° to 50° lines of latitude through Europe and Russia. The southern limit begins in the west in northern Morocco, Algeria, and Tunisia and proceeds east to include all of the Mediterranean islands, on a line through Israel into Asia [98]. The latitudinal distribution of L. dispar in Canada and the United States lies between 35° N and 48° N [91]. Generally, damage caused by L. dispar in Europe increases from west to east and from north to south [123]. Furthermore, due to the projected climate change, L. dispar may be a threat to more northerly ecosystems [35].
The spread of L. dispar in Europe has been recorded in the database of the European and Mediterranean Plant Protection Organization [9]. According to this database, this species is present in Austria with few occurrences. It is present in Belarus, Belgium, Croatia, Denmark, Italy (including Sardinia and Sicilia), Lithuania, Moldova, North Macedonia, Poland, Romania, Serbia, Slovenia, Turkey, Ukraine, and Azerbaijan, where L. dispar has been classified in the A1 list (pests are not present in the EPPO region) since 2007, and in Russia, which has been classified in the A2 (the presence of pests occurs locally in the EPPO region) since 2014. In Spain, there are reports from the XIX century. It is known as “lagarta peluda” in Spain, as “eruga peluda del suro” in Catalonia, and “eruga peluda” in the Balearic Islands. Most of the information available in Spain comes from old pest control books and technical leaflets published by some Spanish Regional Plant Health Services [57,58,66,67].
The dispersal of L. dispar is impressive since its females are not able to fly [12,57,58,59,124,125]. However, the spread of this species in new areas can occur through larvae that can disperse over short distances, as well as through the human-mediated movement, which can help spread some of the life-stages of this pest to over long distances [15,94]. Concretely, dispersal by larvae is accomplished by either their crawling from tree to tree or by larval ballooning, that is, a wind-borne movement, and is therefore limited to short distances (<100 m) [126,127,128,129]. Early instar larvae move to tree crowns, where they hang from strands of silk until the wind carries them locally to other trees, particularly in an urban situation [130]. In some cases, larvae may “balloon” several times before they start feeding [131]. However, it has been reported that the newly hatched larvae have been blown to distances of 56 km [61]. In addition, the primary pathway for the long-distance of L. dispar is human assisted (i.e., recreational travel; transportation of egg masses on firewood, household goods, and vehicles) [29,125,132,133]. For example, L. dispar has spread at a rate of 3 to 29 km per year since its introduction to the USA [134,135], which is based on a dispersal rate of more than 20 km per year for the period between 1966 and 1990 [131]. On the other hand, in the absence of anthropogenic movement, the natural spread that occurs through early instar-larvae ballooning could be as slow as 2.5 km/year [131].
The establishment of L. dispar in a new area depends on the temperature. For instance, in warm climates such as southern Florida, this species is not able to complete a full life cycle because there are not suitably low temperatures to complete the diapause [136]. In addition, in areas where the high summer temperatures exceed the optimum temperatures for larval and pupal development, the probabilities of establishing of this species are low [137,138]. Another important parameter for successful establishment in small, isolated populations or those at low density near range edges is the ability of individuals to successfully locate mates [139,140,141]. More specifically, the failure to establish L. dispar infestations ahead of the invasion is because of the unsuccessful detection of females by the males in low-density populations [139].

3.2. Outbreaks

Lymantria dispar populations appear to exist in one of the following four phases: innocuous, release, outbreak, and decline [94]. The innocuous phase is characterized by very low population levels. The release phase usually takes place over the course of one or two years and can result in population density increases of several orders of magnitude. During the outbreak phase, populations are high enough to cause noticeable defoliation to host trees. After this point, the decline phase follows, which is characterized by high levels of L. dispar mortality usually due to starvation or disease and the population crashes. Outbreaks in the whole area can last up to 10 years, but generally population densities in localized areas remain high for two or three years [142]. Usually, outbreaks of forest defoliators emerge in a synchronous manner at large spatial scales [143]. In contrast, L. dispar asiatica, which is found in Russia [144], exhibits asynchronous population outbreaks. This is because temperature varies considerably in Russia during winter (<−30 °C) vs. other European countries [145]. For several decades, the cyclic population dynamics and their genetic consequences have been an area of interest [146]. Lymantria dispar exhibits cyclic population dynamics [98,147,148]. More specifically, in Europe, which is the native territory of this pest, it exhibits cyclical outbreaks every 8–13 years [148]. For instance, in Spain, it is reported that cyclic outbreaks may last for a couple of years, followed by 7–11 years of non-outbreak period [58,66]. On the other hand, in North America, where the L. dispar is an invader species, it exhibits varying periodicity, every 4–5 years or 8–10 years, depending on forest type [33]. Severe outbreaks of L. dispar larvae can completely defoliate forest canopies, which have many short-term effects. These effects are related to the reduction in productivity or the reduction of seed crops, the increase in light to the forest floor, reduced transpiration that leads to increased water drainage from the forest, and a pulse of nitrogen and labile carbon to the forest floor [6,149,150]. In addition, as the host trees and seedlings can be completely defoliated and killed during outbreaks, this can cause changes in the composition of natural forests [151,152,153]. After an outbreak, L. dispar populations collapse due to viral or fungal disease, parasitism, predation, starvation, or adverse climatic conditions [154]. Apart from the environmental damage caused by the outbreaks of this pest, there are considerable costs in terms of economic losses and the cost of control measures [121,155,156].
Lymantria dispar infestations have positive and negative effects on wildlife. On the one hand, defoliation can lead to increased growth of shrubs, grasses, and herbs, providing an additional habitat for some wildlife species. On the other hand, defoliation may reduce or compromise the habitat for some wildlife species. For instance, bird eggs become vulnerable to predation due to reduced protection following defoliation of the tree leaves. Waterways can also be affected by outbreaks of L. dispar. Loss of canopy cover due to defoliation may increase the temperature of streams, which may be detrimental to aquatic organisms [157].
The most numerous and severe outbreaks have occurred in the Balkan peninsula because of the abundance of oak species and the climate (i.e., high temperatures and humidity deficits), which seems to be the optimum for the development and survival of L. dispar [98]. Indeed, in an earlier study, Schwenke [158] reported that the climate and the affinity of L. dispar for warmth and drought are causing an outbreak in southeastern and southern Europe. However, periodic outbreaks have been recorded since 1600 in Europe [159]. For example, outbreaks were reported in 1600 in Spain, 1750 in Germany, 1840 in Hungary, and 1880 in France [98]. In Serbia, 16 outbreaks were reported between 1862 and 1998, with the largest occurring in 1997 when 500,000 ha were infested [160]. Notably, in the mid-1950s and 1960s, outbreaks of this species were widespread and devastating in Europe, causing 70% defoliation in the Yugoslavian hardwood forests in 1957 [161]. However, the most severe epidemic in Europe took place between 1991 and 1995, affecting seven countries and hundreds of thousands hectares of forests, making control measures imperative [118,162]. During that period, France suffered the most, since this outbreak lasted longer there than in other Central European countries [118], where only in Alsace, an area of 23,500 ha, was defoliated in 1994 [163]. In Austria, 1500 ha were infested by the pest in 1993, causing severe defoliation on 400 ha of oak stands [164], whereas one year earlier in Switzerland, 2000 ha composed mainly of chestnut trees was defoliated. However, after the collapse of the L. dispar population in 1993, the trees recovered without any treatment [165]. An outbreak in Germany affected almost 2000 ha in 1992, while one year later, the infestation covered 47,000 ha, and in 1994, before the natural population collapsed, the pest was present in about 80,000 ha [118]. Furthermore, during this period, small outbreaks occurred in England, where the climate is rather unfavorable for L. dispar [118,166]. In Hungary, 22 outbreaks have been reported between 1843 and 2007, with the maximum damage (i.e., 212 thousand hectares) recorded in 2005 [98].
Lymantria dispar in Greece is considered one of the most important pests of oak trees. Greece has experienced several population outbreaks [167]. More recently, over the years 2016 and 2017, repeated outbreaks have been reported in different parts of Greece (i.e., Macedonia, Ipirus, and Thessaly) on evergreen pastures, where Q. coccifera predominates [130]. In Catalonia (Spain), during the last century, several outbreaks with massive defoliation were recorded, especially on Q. suber from the coastal and pre-coastal mountains of the Transversal Mountain System [168]. After a long period without important damage, new outbreaks were recorded in 2018–2020 in several counties, especially in the natural park of Montnegre-Corredor, in Barcelona province. Soldevila [169] and Stefanescu et al. [59] performed a detailed study in some affected forest of the Montnegre mountains of Catalonia (Barcelona province) where they determined the outbreak effects and the role of natural enemies as biocontrol agents. Defoliation of oak forest by L. dispar has been especially important in the Montnegre-Corredor park on Q. rubra and Q. ilex, after more than two decades without records of massive defoliations [65]. In that area in 2019, the damage covered nearly 15,000 ha [170] and it caused social alarm and concern in the forest owners, as more than 90% of the forest area of Catalonia is private. The attack not only affected Quercus sp., but also many specimens of A. unedo, P. halepensis, Celtis sp., Castanea sp., and other tree species.
During 2006–2008, the territory of the Russian Far East suffered from a L. dispar outbreak, which was characterized as the most severe since the 1930s [171]. In the Ugam-Chatkal range of Uzbekistan, 500 ha of various forest and fruit tree species were heavily damaged by L. dispar [172]. Furthermore, L. dispar outbreaks were reported in Northern Kazakhstan in 2017, damaging 247 ha of forest plants [173]. In North America, the history of outbreaks is related to the dispersal of L. dispar in new areas, where the preferred plant species predominate, followed by the rapid spread of populations due to the absence of a natural enemy complex. After a massive outbreak that occurred in 1979–1982, in 1981, at the peak of the outbreak in the USA, L. dispar defoliated more than 6 million ha of forests [174]. Later, the next outbreak occurred from 1989 to 1993, affecting forest areas in 12 different states [98].

4. Control of L. dispar

Lymantria dispar is considered one of the most destructive invasive pests, ranking third among the most costly invader insect pests worldwide [153]. Defoliation by L. dispar larvae can cause tree biomass losses up to 70%, while cumulative effects can result from consecutive defoliations [175,176]. From an economic perspective, L. dispar can massively affect timberlands and agricultural products, with high yearly costs on quarantined products. This pest impacts the aesthetics of forests and property values in urban areas, imposing high costs (disinfestation, tree removal, and replacement); it also burdens health systems and may negatively affect tourism. For instance, in the USA, the economic impact of this species was estimated at about USD 250 million per year in 2011 [121], but with the continued spread of L. dispar in North America, the economic impact was increased to USD 3.2 billion per year in just a few years [155].
In years with moth outbreaks, cutaneous reactions in humans can reach epidemic proportions in communities located near infested trees, the contact with airborne setae being mainly responsible. It is, therefore, crucial to control and manage L. dispar to mitigate the possible ecological, economic, and social impacts. Due to the negative impact of L. dispar on the forests, several pest control programs have been conducted against this pest to reduce populations and damage during outbreaks [177,178] or to slow its spread from infested to uninfected areas [134,179,180,181]. The first tools to control L. dispar were crude. Early trapping devices were baited with live females and other control tools were oil-fueled flamethrowers to destroy the life stages and microhabitats of the pest, as well as arsenic-based insecticides (copper acetoarsenite and lead arsenate) [52]. Current control measures include chemical and mechanical methods, natural predators, and silvicultural practices. In addition, the economic damage threshold of 100 egg clusters per 40 trees, which are equivalent to an average number of 2.5 egg clusters/tree, is used to make decisions about the initiation of management tactics [182,183,184].
The use of conventional insecticides, such as organophosphates, carbamates, and pyrethroids, is common in pest control, especially to prevent the spread of destructive insect species such as L. dispar, but this approach can be harmful to human health and the environment [185,186,187]. Although there is an increasing demand for alternative eco-friendly methods to control L. dispar (e.g., viruses, parasites, pheromones, fungi, or bacteria), chemical control is still the most common and effective method [188,189,190,191]. Starting from the 1980s, broad-spectrum insecticides used for L. dispar control have been replaced with bioinsecticides based on entomopathogenic viruses, bacteria, and fungi, as well as technologies such as mating disruption using sex pheromone traps [192,193].

4.1. Biological Control

4.1.1. Natural Enemies

The infestation levels that L. dispar can cause in North America are much higher than those in Europe, due to more suitable biotic and abiotic conditions in the newly invaded areas [98]. Apparently, this phenomenon is partially due to the fact that its natural enemy complex in Europe is much more diverse than that in the Nearctic region, so that the natural regulation (i.e., naturally occurring biological control) of L. dispar populations is more efficient in Europe than in North America. The natural enemies include various predators, such as small mammals and birds. However, small mammals and birds do not come in numbers able to control large populations because the pest reproduces much faster than the predators. Pathogenic fungi require specific conditions to germinate and infect L. dispar larvae (high humidity, rainfall), making their effectiveness in a given year subject to local weather conditions. The natural enemies of L. dispar are presented in Table 2.
When the presence of L. dispar in an oak forest is at a high density, it becomes part of the food chain and can be an important food source for birds and small mammals (e.g., rodents) [194,204]. For instance, P. leucopus, which feeds on L. dispar larvae and pupae, can regulate low-density populations of this pest [194]. Moreover, mice can cause high mortality, for example, they killed 98% of deployed L. dispar pupae within 72 h in Ukraine [98] and caused more than 45% mortality in an artificial population of L. dispar pupae in Austria [205]. However, the abundance of small mammals and predation rates are affected by forest types and altitudes [206,207].
Recenlty, Soldevila [169] and Stefanescu et al. [59] considered the role of natural enemies in their studies in Catalonia. The authors identified A. sylvaticus and C. russula as predators with the capacity to maintain populations of L. dispar at low densities. As the abundance of small rodents is linked to the abundance of acorns, they suggested that after several years of low abundance of the fruits, the populations of rodents would decrease, allowing an increase in L. dispar populations.
In earlier studies, birds had been proven to be one of the most important predators [194,208,209,210,211]. For instance, bird predation damaged 77% of the egg masses in Slovakia [208]. The predation rates of egg masses by birds in North America are between 65% and 89% [98,212]. Soldevila [169] and Stefanescu et al. [59] also reported the potential role of P. major, G. glandarius, D. kizuki, and S. eiuropaea.
Calosoma sycophanta is a predatory beetle that is known to occur in high densities during outbreaks of L. dispar [56,195,196,197,198,199]. Adults and larvae of this species are the main predator of larvae and pupae of L. dispar [98,213,214]. It is distributed in the Western Palearctic, covering the whole of Europe, northwest Africa, and Western and Central Asia [200,201,202,203]. It was imported from Europe to the USA as a natural enemy of L. dispar in 1906 and is now a well-established predator [214,215,216,217]. It has been reported that a pair of C. sycophanta adults and their offspring can predate more than 6000 L. dispar larvae and pupae within one season [198].
Stefanescu et al. [59] and Soldevila [169] reported the occurrence of C. sycophanta in Catalonia, confirming its capacity of this prey upon the larvae and pupae, as also reported by Weseloh [196]. Calosoma sycophanta was able to predate a large number of L. dispar when the density was high, but its role was much less important when L. dispar density was low. The above-named studies also stated that the parasitoids of the genera Anastasus, Cotesia, Exorista, and Brachymeria were present in the study area. However, vertebrates are more likely to cause high mortality than invertebrates [211]. In Slovakia, for instance, invertebrates caused 38% of egg mass predation, while vertebrates caused 62% [211]. In general, it has been suggested that predation by small mammals is able to keep L. dispar populations at low densities [205,206]. However, outbreaks occur at intervals, presumably due to human transfer of life stages of L. dispar from an infested to an uninfested area [132].
In the USA, since the early 20th century, numerous attempts have been carried out to eradicate or suppress the dispersal of L. dispar, but none have prevented the continued spread of the pest to the south and west of the country. Among the attempts was the development of a biological control program. The guiding philosophy for biological control in North America was to establish there all the natural enemies that attack L. dispar in Europe [218]. Thus, such a program mainly involved the introduction, rearing, and release of L. dispar enemies from Europe [198,218]. At least 20 parasitoids and predators have become established, but they have still been unable to control the moth populations [127]. By 1933, nine natural enemies of L. dispar had become established in North America. One of these was C. sycophanta, as well as some small hymenopterous egg parasitoids and some tachinid flies that attack the large larvae of L. dispar [219]. In addition to the other natural enemies in Europe, there are a large number of parasitoids that are able to attack L. dispar; of these, 109 species belong to the order Hymenoptera and 56 species belong to the order Diptera [63]. Despite this diversity of parasitoids, efforts have been conducted to establish parasitoids in the invasive range of L. dispar, but only a few parasitoid species can be considered as established there [50,83,220,221].

4.1.2. Bioinsecticides or Pathogens

Among the control methods developed against L. dispar [222], the application of bioinsecticides has proven to be a successful approach for the control of this pest, with a low environmental impact [36,223]. Aerial applications of formulations based on the entomopathogenic bacterium Bacillus thuringiensis Berliner serovar kurstaki (Btk) exploit the highly specific mode of action of bacterial toxins that selectively target moth larvae [224]. This method is currently the most frequently used and effective to suppress L. dispar outbreaks since it has few biological and practical limitations [225]. However, there is some evidence of side effects on non-target Lepidoptera that live in the forest ecosystem [226].
Several factors should be taken into account to increase the effectiveness of Btk applications against L. dispar [227], including the timing of application relative to the phenology of second instar larvae [228,229], dose [180,230], the size of droplet, and density on foliage of insecticides based on Btk [231].
Stefanescu et al. [59] evaluated the defoliation that occurred in plots of a damaged area in 2020 on trees that had been already attacked or not in 2019. The cumulated defoliation that occurred in 2020 (2019 + 2020 damage) was estimated at 20% to 60%. As a measure to reduce damage, the Plant Health Services of the Department of Agriculture of the Catalonia Government planned a program based on the treatment of the most affected forests with Btk, and around 2500 ha were sprayed in order to maintain the productivity of the forest, especially areas of Q. suber exploited to obtain cork. The cost of spraying was estimated at 50 EUR/ha. The efficacy of such treatments was low and did not have any significant effect on the reduction of defoliation [59], and the use of Btk spraying for controlling damage of L. dispar was seriously questioned. Several reasons were given: (1) the development of the larval population in one locality is not synchronous and there are several larval instars the at the same time; (2) the negative effect that the treatment may have on the non-target species: although Btk is a selective bioinsecticide widely used in integrated pest management, it negatively impacts lepidopteran larvae and some predator species such as the green lacewing Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae) [59]. Indirectly, the reduction of lepidopteran larvae in sprayed Btk areas can lead to a reduction in the natural enemies that feed on them. This last aspect of loss of biodiversity is more relevant in protected areas such as the Montnegre of Catalonia. Although the study of Stefanescu et al. [59] did not measure and compare the productivity of sprayed and unsprayed forest, they argue that Q. suber forest has a notable resilience to L. dispar outbreaks.
During the outbreak of the 1990s in central Europe, control measures against L. dispar in France (1995 epidemic) were carried out in an area of 2500 ha using Btk. In Slovakia and the Czech Republic in the 1993–1994 outbreaks in oak forests, treatments with Btk were necessary. In Germany, in the outbreaks of 1993 and in 1994, Btk was applied by helicopter to infested areas. However, mainly due to adverse weather conditions, this treatment failed to provide sufficient protection on the affected forest stands [118]. More recently in Greece, the field treatments with Btk against L. dispar showed that this biopesticide caused 66% mortality to the second instar larvae after 4–5 days [36].
Lymantria dispar has been treated with other biocontrol agents such as entomopathogenic fungi and entomopathogenic nematodes [36,38,39,40,41,42,43]. The entomopathogenic fungus Entomophaga maimaiga Humber, Shimazu and Soper 1988 (Entomophthoromycota: Entomophthorales) was introduced to the United States from Japan for the biological control of L. dispar in the early 1900s; however, its introduction was unsuccessful [232]. Much later, in 1989, there was an unexpectedly high percentage of dead larvae due to this fungus [233,234], probably because it had been accidentally introduced to North America after 1971 [235]. In late 1990s, E. maimaiga was introduced to Bulgaria from North America [236]. Since then, it rapidly spread across Europe, indicating that this continent is suitable for the survival and development of the fungus [237]. Field studies in Europe documented that L. dispar larvae exhibited 98% mortality when infected by E. maimaiga [238,239,240], suggesting the high potential of this fungus to become an important management tool [237]. The entomopathogenic nematode Steinernema carpocapsae (Weiser, 1955) (Rhabditida: Steinernematidae), which was used for the first time in Greece in field trials against this pest, killed 69% of the second instar larvae, indicating that it has a great potential as a control agent [36].
Another group of entomopathogens is the baculoviruses that are very specific microorganisms [241] that cause fatal infections to larvae after the ingestion of viral particles. The bioinsecticidal activity is associated with crystalline occlusion bodies that, after their ingestion by susceptible insects, release occlusion-derived viruses (ODVs) that infect the host midgut epithelial cells. The production of a second type of virions, namely, budded viruses (BVs), responsible for the infection spread in the host body [242]. The Lymantria dispar multiple nucleopolyhedrovirus (LdMNPV) is very specific to this pest and is therefore environmentally safe. It was apparently introduced accidentally with L. dispar in North America [243]. This virus naturally causes epizootics, resulting in the decline of the pest population after two or three years of outbreaks [244]. For instance, Kurenshchikov et al. [171] reported that LdMNPV suspended the population of L. dispar after the outbreak in Khabarovsk Krai (Far East region of Russia) in 2006–2008. However, it can be produced in large quantities only by infecting live L. dispar larvae. Thus, it is produced in limited quantities, sufficient only to treat <550 km2 per year [125]. At first, virus production was costly since efficient host larval breeding techniques were limited [245]. However, research efforts have revealed that virus yields can be increased by using late-instar (i.e., fifth instar) female larvae where, in combination with new larval processing methods (i.e., using freeze-dried, intact larvae), the cost of the production of the virus can be reduced effectively [245]. The USDA Animal and Plant Health Inspection Service and the Forest Service have investigated practical ways to use the virus as biological insecticide. Thus, it was registered with the Environmental Protection Agency in 1978 as Gypchek [243]. Lewis and Yendol [246] reported that Gypchek adequately controlled L. dispar in forest trials. In addition, in North America, the virus is considered to be the most significant factor causing the collapse of L. dispar populations [98]. More recently, Ruiu et al. [247] suggested a multi-year integrated program that would include the combined use of Btk to reduce infestations and nucleopolyhedrovirus in order to regulate population dynamics. The disease is often referred to as “wilt” because of the soft, limp appearance of diseased larvae [11].
Lymantria dispar can host several microsporidian pathogens, some of which have been considered for inoculative releases in North America [248]. Vairimorpha disparis (Microsporidia, Burellenidae) and Nosema lymantriae (Microsporidia, Nosematidae) infect L. dispar larvae when the spores are ingested on food. The developmental cycle begins in the midgut and eventually leads to the formation of primary spores [217]. Vairimorpha disparis is a parasite of the fat body. The environmental spores are transmitted between host larvae and can be found in the fat body after 7 days. After 10 days, the fat body is full of spores, and under laboratory conditions, an infected larva dies on average 4 weeks after infection [249]. Horizontal transmission takes place when spores are released from the decomposing cadaver. Nosema lymantriae is a systemic parasite that affects the silk glands, the fat body, the gonads, and the Malpighian tubules of a host larva. Most of the infected larvae will die 4 weeks after infection. Horizontal transmission of this species begins after the end of the latent period when the spores are released with feces about two weeks after infection, and also continues after the death of the host larva when its cadaver decomposes [249]. Furthermore, infected females can transmit Nosema lymantriae transovarially to their offspring [250].
In Central Europe, it has been reported that pathogens can cause higher mortality than parasitoids [208,251,252]. Since entomopathogens can act against L. dispar, Stephanescu et al. [59] reported that it is probable that the baculovirus LdMNPV is present in Catalonia, although there are no records of this. In conclusion, it seems that natural enemies play a role in maintaining L. dispar populations under outbreak thresholds or in reducing population levels after outbreaks.

4.2. Traps and Attractants

The development of the sex pheromone cis-7,8-epoxy-2-methyloctadecane (disparlure) that attracts L. dispar males took place in the 1970s [253,254]. The existence of the pheromone was known in the early 1900s, and the tips of the female abdomen were extracted into organic solvents to provide pheromone that could be used in trapping research as early as 1932 [255]. This pheromone has been used extensively for the detection of this pest [134] and is able to attract all of the different subspecies of L. dispar [12]. The commercially available pheromone disparlure provides an extremely sensitive and host-specific research tool that is effective even when moths occur at very low population densities [6,256,257,258]. Without such a sensitive trapping tool, it would be extremely difficult to engage in management efforts that depend on early detection [125]. The detection of low-density populations of this pest is essential for eradication campaigns. Moreover, pheromone-baited traps are effective at both low and high densities, and this method is considered the most sensitive method for detecting L. dispar [15].
The sexual behavior of males [244,259], as well as the physical characteristics of a trap, such as the shape, size, color, and the location of entry ports, must be taken into account when designing a trap [6]. There is a wide variety of pheromone trap designs from disposable cardboard traps with a sticky inner surface to various canister-type or “milk carton” traps made of cardboard or reusable plastic that contain an insecticide to kill the captured moths [11]. Strategies to slow the spread of L. dispar are based on pheromone traps for detecting and delimiting small, isolated populations immediately after establishment [193,260]. These infestations can then be targeted for mass trapping, mating disruption, application of microbial insecticides, or other appropriate methods to limit the population growth and spread of the pest [261,262,263].
Mating disruption (MD) has long been regarded as a viable option for non-chemical control, especially in the case of Lepidoptera [264]. For MD, artificial male pheromone is released in a treated area in order to compete with pheromone produced by calling females, and this can drastically reduce mate finding by males and thus mating [265]. Currently, this method is used to control a large number of insect pest species, mainly lepidopteran species, but not exclusively so [264,265,266,267,268,269,270,271,272]. MD has been successfully marketed for a very wide range of moth species of economic importance [273,274,275].
With this method, mating may be delayed, which contributes to reduced fecundity [276,277] and egg fertilization [277]. Moreover, MD can reduce the risk of insecticide resistance because mating among resistant individuals is decreased [278,279,280]. Since the target organism is not killed by this method, non-targeted effects are believed to be rare [179]. It is also compatible with other pest management strategies, such as biological control [261]. The discovery of disparlure also helped to develop and optimize host-specific MD tactics that are also considered a very useful control tool [193,254,269].
MD has been proven to be effective against low-density populations of L. dispar in the USA [179,281,282,283,284]. On the other hand, it may not work in high-density populations where female moths are abundant and easy for males to locate, making it ineffective without the combined use of other control measures. As a univoltine species, L. dispar is ideal for MD, as a single annual application may lead to rapid population suppression, without the need to reapply the method; however, the timing of the application is critical, i.e., before males mate with females. Although L. dispar is a serious threat for both the environment and human health, the MD method has never been evaluated on a large scale in Europe as a reliable management tool.
An alternative control method is the use of trunk barriers, which can take advantage of the dispersal behavior of the larvae [80]. The use of burlap bands wrapped around the trunk is an old technique that helped to collect and destroy the larvae [52]. In the early 1900s, the protection of trees from L. dispar in Massachusetts was based on the extensive use of sticky barrier bands [285]. Later, burlap bands and similar devices were used to detect and monitor L. dispar populations [84,286,287]. For instance, burlap bands that were placed around the base of the trunk have been used to trap and monitor late-instar larvae; the larvae use the burlap bands as a preferred resting site during the day [288]. Moreover, the first-instar larvae that move upward on the tree stem after hatching can be trapped in the sticky barrier bands [289,290].

4.3. Chemical and Biorational Control

There are only a few insecticides registered for L. dispar control in Europe, such as insect growth regulators (IGRs), which are biorational products, and Spinosad, a naturally derived product [36,37]. Other insecticides may be used to effectively control L. dispar, but since their potential harm to other species is considered too high, they are not recommended for widespread use. In the past, the application of pesticides to prevent L. dispar attack has been shown to have a greater effect on the bird populations than on L. dispar themselves [291]. Moreover, since this species may occur in urban/recreational areas, chemical control is even more challenging as many of the registered pesticides cannot be used due to risks of exposure to mammals. Prior to 1966, area-wide eradication programs by spraying with dichloro diphenyl trichloro ethane (DDT) were considered effective. However, DDT and similar insecticides were eventually banned due to environmental concerns about their toxic effects becoming recognized, leading to research in finding alternatives to broad-spectrum synthetic pesticides [292].
In North America, massive aerial applications of pesticides have been made against L. dispar populations, aiming largely at suppressing their outbreaks [192]. For instance, the application of chemical pesticides (e.g., DDT) to millions of acres of forest in the United States took place annually during the 1940s and 1950s [293]. In the United States, the chemical insecticide diflubenzuron, which is a molting disruptor, was widely used during the 1980s [182] and in some European forests until recently [294]. For example, in Slovakia and the Czech Republic in the 1993–1994 outbreaks, the application of diflubenzuron in oak forests was used to control this pest. In Germany, the same treatment was applied to three-quarters of the infested area, which was proven to be more effective than treatment with Btk [118]. Although this insecticide is not toxic to vertebrates, concerns have been raised about its adverse effects on invertebrates [295] and the potential effects of the 4-chloroalinine metabolite on human health [296]. Later, tebufenozide, which is a molting hormone agonist, was approved as an alternative to diflubenzuron due to its specific action on Lepidoptera [178]. This compound now plays an important role in L. dispar management in the United States [89]. It is also the preferred option for some European countries (e.g., Germany) because of its reliable suppression of L. dispar populations [297].
In a recent study conducted in northern Greece, Papadopoulou et al. [36] reported that a product containing 24% metaflumizone had a rapid action (1–2 days) against second-instar larvae of L. dispar, causing 88% mortality, while an IGR containing 15% teflubenzuron was less effective, killing 76% of second instar larvae. In Spain, the authorized insecticides comprise azadiractin, cypermetrin, and indoxacarb [66]. Spraying with aircraft or some other flight system can only be performed by government Plant Health Services. The semi-synthetic bioinsecticide emamectin benzoate (EMB), which is derived from naturally occurring avermectin, is a widely used control agent for agricultural and forestry pests [298,299]. The determination of the sublethal concentrations of EMB and their effects on L. dispar was conducted by Xu et al. [300]. These authors found that sublethal concentrations of EMB can inhibit the growth of larvae, which is related to midgut damage, digestive dysfunction, and nutritional metabolism disorders. They also provided a theoretical basis for understanding the sublethal effect of EMB and its application to the prevention and control of L. dispar. According to Cannon et al. [166], an eradication program was applied in the UK, including three axes: (1) investigation for detecting egg clusters or larvae, and captures of adults using pheromone traps; (2) chemical treatments of larvae; and (3) extensive information of the public about the importance of the pest. This procedure resulted in a decrease in the captures of adult males in comparison with the captures of the first two years of the program.
In the past decade, increasing attention has been paid to the development of insecticides based on unmodified nucleic acid fragments, with an emphasis on antisense DNA fragments [301,302] and double-stranded RNA fragments [303,304]. These insecticides are considered to be the next-generation control agents that have numerous advantages over broad-spectrum products. They can combine the affordability and rapid action of chemical insecticides combined with the selectivity of biological preparations. The nucleic acid synthesis technologies are becoming less expensive, making DNA insecticides and RNA preparations increasingly economical, and their affordability can be compared to that of chemical insecticides. So far, antisense DNA-based insecticides are the only nucleic acid preparations being developed to control L. dispar [305].
Recently, Oberemok et al. [306] suggested a novel biotechnology for pest control, using a DNA insecticide that has improved insecticidal action based on a new antisense oligoRIBO-11 sequence from the 5.8S ribosomal RNA gene. This novel insecticide caused high mortality among L. dispar larvae reared in the laboratory and those collected from the forest. Furthermore, the insecticidal potential of three different 10–12 nucleotide long antisense sequences from the 5.8S ribosomal RNA gene of L. dispar against its larvae was compared. The results showed that antisense fragments of 10 and 11 nucleotides (oligoRIBO-10 and oligoRIBO-11) caused higher larval mortality than the 12 nucleotide long fragment (oligoRIBO-12) [307]. In addition, this oligoRIBO-11 insecticide was more affordable and acted faster than the previous preparations developed by Oberemok et al. [307], according to longer antisense fragments of anti-apoptosis genes of the baculovirus–host system.

4.4. Essential Oils

Many insecticides have been removed from the market due to the development of resistance and the severe environmental disturbances (i.e., persistence of residues and adverse effects on non-target organisms) [308,309,310,311,312,313]. Intensive work is being done to find alternative environmentally friendly pest control methods that will be effective [314,315,316,317,318,319]. In this context, plant-based products have been considered as potential control agents for pests, including L. dispar [320,321]. Recently, plant essential oils (EOs), which are complex mixtures of compounds that act as a defense agents against pests and pathogens and provide protection to the plant from heat and cold have attracted attention [322,323]. EOs are also generally recognized as safe biopesticidal agents [324,325,326,327,328].
Several EOs can be promising “green” alternatives to chemical insecticides for the control of L. dispar, as they have been examined under laboratory conditions. For instance, Moretti et al. [329] found a high digestive toxicity of rosemary, Rosmarinus officinalis L., and thyme, Thymus herba-barona Loisel. (Lamiales: Lamiaceae), EO emulsions to second and third instar larvae of L. dispar after 3 days of exposure. In addition, the EOs from basil, Ocimum basilicum L. (Lamiales: Lamiaceae); Athamanta haynaldii L. (Apiales: Apiaceae); and nutmeg, Myristica fragrans Houtt. (Magnoliales: Myristicaceae) had low to moderate residual contact and digestive toxicity, but they had good antifeedant activity against second instar larvae [3,330].
More recently, Devrnja et al. [331] examined the effect of the EO of the tansy, Tanacetum vulgare L. (syn. Chrysanthemum vulgare L.) (Asterales: Asteraceae), at three concentrations (i.e., 0.1, 0.5, and 1% v/v), on the survival and molting of second-instar larvae, as well as on the nutritional indices of the fourth-instar larvae of L. dispar. Exposure of the second instar larvae to tansy EO (residual contact toxicity) caused low mortality (<10%), but larval development was significantly extended, i.e., the proportion of larvae that molted into the third instar was decreased after 120 h of exposure in comparison with the control larvae (92% molted into the third instar). Consequently, delayed ecdysis, which is associated with prolonged growth, could extend the period for which larvae are exposed to their natural enemies. However, in a digestive toxicity assay in which tansy EO was incorporated into the diet, the highest concentration of the EO (i.e., 1% v/v) caused high mortality and a lack of molting after 120 h of consumption. Oxygenated monoterpenes were the predominant group of compounds with 93.5% in tansy EO [331,332]. Terpenes can act as deterrents or toxicants to L. dispar larvae [333], indicating that compounds from EOs could be isolated and used for the control of this species. However, the sensitivity of exposed larvae depends on the terpene structures and larval age [331].
Kostić et al. [321] evaluated the impact of different concentrations of essential oils (EOs) from the seeds of three Apiaceae plants, namely, anise, Pimpinella anisum L.; dill, Anethum graveolens L.; and fennel, Foeniculum vulgare Mill. (Apiales: Apiaceae), on the behavior, mortality, molting, and nutritional physiology of L. dispar larvae. The authors also compared EO efficacy with the commercial insecticide NeemAzal®-T/S (neem). Their results showed that the tested EOs may be a promising strategy for L. dispar control since they provided strong negative effects on survival and consumption in second-instar larvae and impairment of nutritional physiology in fourth-instar larvae. Anise EO was proven to be the best antifeedant, while dill EO caused the highest mortality. In addition, at the concentration of 0.5%, the three EOs performed better than the commercial insecticide neem in reducing relative growth rate, efficiency of conversion of ingested food, approximate digestibility, and efficiency of conversion of digested food of the fourth instar larvae of L. dispar. Although essential oils represent an eco-friendly management tool, their cost is high.

5. Public Health Concerns

Envenomation (i.e., infusion of an insect secretion into a human’s body) caused by moth or butterfly larvae in humans is known as “erucism” or “caterpillar dermatitis”, coming from the Latin “eruca”, which means caterpillar [334]. This kind of dermatitis has been noted since ancient Greek times [88,113,335]. Caterpillar envenomation constitutes a serious public health issue of international importance [336].
The setae of the caterpillars, which are filled with toxins (such as proteolytic enzymes, histamine, and other pro-inflammatory substances), are responsible for the allergic reactions they cause to humans or to animals [337,338,339,340]. The bristles are able to penetrate the subcutaneous tissue and release toxins [336,341], causing cutaneous reactions, such as immediate severe pain, erythema, and edema [336]. Of the three types of urticating hairs that exist in Lepidoptera, L. dispar larvae have modified setae [342]. The presence of histamine has been reported in the setae of L. dispar larvae [343,344,345,346,347]. In addition, histamine or histamine analogues have been isolated in other lepidopteran species of medical importance found in Europe, such as the pine-tree lappet moth, Dendrolimus pini (L.) (Lepidoptera, Lasiocampidae), and the browntail moth, Euproctis chrysorrhoea L. (Lepidoptera: Lymantriidae) [348]. Moreover, first instar larvae of L. dispar carry setae that are impregnated with nicotine, while this substance occurs in a lower concentration in last instar larvae [342,349].
It has long been recognized that L. dispar can cause dermatitis in humans [350], especially in laboratory staff [351]. In addition, the early instar larvae are considered more allergenic than mature larvae [130,352]. Several studies have shown that a large proportion of workers in breeding facilities of this species for experimental purposes developed pruritic urticaria on exposed skin after contact with its larvae [353,354]. Other symptoms associated with allergic reactions to larvae are eye irritation, rhinitis, and shortness of breath [354,355].
Very little information is available on the prevalence of cutaneous reactions focusing on children and in the general adult population. The first community-wide outbreak of L. dispar dermatitis was reported in the United States in 1981 [343]. That year, a massive outbreak of larvae was recorded in northeastern United States during spring [356], where people outdoors came in to contact with first instar larvae [352]. Thousands of people presented skin irritation, which was described as unusual pruritic dermatitis with stinging, while some people had respiratory difficulties [343,345]. Moreover, the skin lesions of the patients’ occurred within 12 h of contact with L. dispar larvae [343,345,352,357]. After the outbreak of 1981, there were no other reports of an allergic reaction to this pest [357] until the spring of 1990, when six new cases with clinical and histopathological features were described [88]. In addition to skin irritation, respiratory problems (e.g., rhinitis or shortness of breath and eye irritation) were reported [88,358].
Although larvae cause dermatitis with a pruritic eruption that lasts from 4 to 7 days, very few clinical and epidemiological studies have been conducted in this species [348,352,359]. Moreover, the etiology of L. dispar erucism and lepidopterism has not been fully clarified [115,357]. An epidemiologic study was carried out during the outbreak of L. dispar in 1981 that compared a severely infested and a lesser infested area [353]. The authors found that the highest risk factors for developing L. dispar dermatitis were previous history of hay fever, a history of a similar rash a year ago and direct physical contact or indirect exposure (e.g., hanging laundry outdoors) [352,353,355]. Furthermore, Beaucher and Farnham [345] conducted patch testing using the hairs of L. dispar larvae in 8 patients with a history of L. dispar dermatitis as well as in 11 persons without history that were used as controls. Generally, patch testing with moth or larvae setae revealed the presence of an immediate hypersensitivity, delayed-type hypersensitivity, or both [360]. In all patients with a history of dermatitis, patch testing caused delayed papulovesicular reactions, while only 1 out of 11 controls reacted, indicating a delayed-type hypersensitivity response [345]. Consequently, the mechanism of L. dispar erucism and lepidopterism probably involves local and pulmonary histamine release and delayed-type hypersensitivity reactions in susceptible persons [115,358]. In cases of L. dispar dermatitis, patients receive topical and parenteral antihistamines, oral or parenteral corticosteroids, and bronchodilators (as indicated for bronchospasm) [115].

6. Conclusions and Future Perspectives

Lymantria dispar is a pest of economic importance that can seriously disrupt forest ecosystems worldwide [361]. Considering the elevated environmental and economic impact of this species, a holistic approach is required rather than ad hoc interventions. In support of this, the European Directive 2009/128/CE of the European Parliament and of the Council of the European Union have established a framework for action so as to achieve sustainable use of pesticides, i.e., reducing their risks and impacts on human health and the environment. This framework promotes the use of integrated pest management (IPM) and the use of alternative non-chemical approaches or techniques [362]. Risks from exposure to chemicals in public parks, gardens, sports and recreational areas, school grounds, children’s playgrounds, or areas close to healthcare facilities are high and should therefore be minimized or prohibited. New approaches regarding monitoring and predicting outbreaks and controlling high-density populations should be introduced in forest and urban habitats. For example, novel trap types should be designed and tested extensively for the capture of larvae and adults. These trap devices can be incorporated in trap monitoring systems that will optimize trap captures at the very early beginning of the presence of the insect. Thus, effective management approaches should be applied accurately, such as the mating disruption method. For this purpose, the European Commission has initiated financial support to universities, research institutes, and private companies to work simultaneously in large-scale field experiments towards the development effective management methods against this serious pest.

Author Contributions

Conceptualization, M.C.B., N.G.K. and C.G.A.; validation, M.C.B., N.G.K. and C.G.A.; investigation, M.C.B., N.G.K., A.S., X.P., C.L.A., M.E., T.B., S.T., E.B.F., E.D.S., S.F., P.A. and C.G.A.; data curation, M.C.B., N.G.K. and A.S.; writing—original draft preparation, M.C.B. and N.G.K.; writing—review and editing, M.C.B., N.G.K., A.S., X.P., C.L.A., M.E., T.B., S.T., E.B.F., E.D.S., S.F., P.A. and C.G.A.; visualization, M.C.B., N.G.K. and C.G.A.; supervision, N.G.K.; project administration, M.C.B. and N.G.K.; funding acquisition, M.C.B., N.G.K. and A.S. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by the EU grant “Using smart traps and pheromones to control the gypsy moth: ecofriendly control in practice” (eGYMER: LIFE20 ENV/GR/000801).

Data Availability Statement

Data are contained within the article.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. De Beurs, K.M.; Townsend, P.A. Estimating the effect of gypsy moth defoliation using MODIS. Remote Sens. Environ. 2008, 112, 3983–3990. [Google Scholar] [CrossRef]
  2. Mull, A.; Spears, L.R. Spongy Moth (Lymantria dispar dispar Linnaeus); Utah State University Extension and Utah Plant Pest Diagnostic Laboratory: Logan, UT, USA, 2022. [Google Scholar]
  3. Kostić, M.; Popović, Z.; Brkić, D.; Milanović, S. Larvicidal and antifeedant activity of some plant-derived compounds to Lymantria dispar L. (Lepidoptera, Lymantriidae). Bioresour. Technol. 2008, 99, 7897–7901. [Google Scholar] [CrossRef] [PubMed]
  4. Milanović, S.; Lazarević, J.; Popović, Z.; Miletić, Z.; Kostić, M.; Radulović, Z.; Karadžić, D.; Vuleta, A. Preference and performance of the larvae of Lymantria dispar (Lepidoptera: Lymantriidae) on three species of European oaks. Eur. J. Entomol. 2014, 111, 371–378. [Google Scholar] [CrossRef]
  5. Cao, C.; Sun, L.; Wen, R.; Shang, Q.; Ma, L.; Wang, Z. Characterization of the transcriptome of the Asian gypsy moth Lymantria dispar identifies numerous transcripts associated with insecticide resistance. Pestic. Biochem. Phys. 2015, 119, 54–61. [Google Scholar] [CrossRef]
  6. Doane, C.C.; McManus, M.L. The Gypsy Moth: Research toward Integrated Pest Management (No. 1584); US Department of Agriculture: Washington, DC, USA, 1981. [Google Scholar]
  7. Mihajlović, L.J.; Grbić, C.; Vandić, D. The latest outbreaks of gypsy moth, Lymantria dispar L., in the region of Serbia in the period 1995–1998. The gypsy moth outbreaks in Serbia. Acta Entomol. Serb. 1998, 80–88. [Google Scholar]
  8. Lowe, S.; Brone, M.; Boudjelas, S.; De Poorter, M. 100 of the World’s Worst Invasive Alien Species. A Selection from the Global Invasive Species Database; Hollands Printing Ltd.: Auckland, New Zealand, 2000. [Google Scholar]
  9. EPPO (European and Mediterranean Plant Protection Organization). EPPO Global Data Base. Lymantria dispar. Available online: https://gd.eppo.int/taxon/LYMADI/categorization (accessed on 6 September 2022).
  10. Fabel, S. Effects of Lymantria dispar, the Gypsy moth, on broadleaved forests in eastern North America. Restor. Reclam. Rev. 2000, 6, 1–15. [Google Scholar]
  11. Nealis, V.G.; Erb, S. A Sourcebook for Management of the Gypsy Moth; Canadian Forestry Service, Great Lakes Forestry Centre: Sault Ste. Marie, ON, Canada, 1993; p. 47. [Google Scholar]
  12. Pogue, M.; Schaefer, P.W. 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; Forest Health Technology Enterprise Team: Washington, DC, USA, 2007. [Google Scholar]
  13. Humble, L.; Stewart, A.J. Gypsy Moth. Natural Resources. Available online: http://cfs.nrcan.gc.ca/pubwarehouse/pdfs/3456.pdf (accessed on 6 September 2022).
  14. Keena, M.A. Identification of Gypsy Moth Larval Color Forms. NE/NA-INF-123-94. Available online: http://www.forestpests.org/gypsymth (accessed on 6 September 2022).
  15. Hajek, A.E.; Tobin, P.C. North American eradications of Asian and European gypsy moth. In Use of Microbes for Control and Eradication of Invasive Arthropods; Hajek, A.E., Glare, T.R., O’Callaghan, M., Eds.; Springer: New York, NY, USA, 2009; pp. 71–89. [Google Scholar]
  16. Metzger, M.J.; Bunce, R.G.H.; Jongman, R.H.G.; Mucher, C.A.; Watkins, J.W. A climatic stratification of the environment of Europe. Glob. Ecol. Biogeogr. 2005, 14, 549–563. [Google Scholar] [CrossRef]
  17. Liebhold, A.M.; Gottschalk, K.W.; Muzika, R.M.; Montgomery, M.E.; Young, R.; O’Day, K.; Kelley, B. Suitability of North American tree species to the gypsy moth: A summary of field and laboratory tests. In U.S. Department of Agriculture Forest Service NE Forest Experimental Station General Technical Bulletin, NE-211; U.S. Department of Agriculture: Washington, DC, USA, 1995. [Google Scholar]
  18. Tobin, P.C.; Liebhold, A.M. “Gypsy moth”. In Encyclopedia of Biological Invasions; Simberloff, D., Rejmanek, M., Eds.; University of California Press: Berkeley, CA, USA, 2011; pp. 298–304. [Google Scholar]
  19. Kozhanchikov, I.V. Gypsy moth. In Fauna Sssr. Nasekomye Cheshuekrylyye. Volnyanki Orgyidae; Izd.AN SSSR: Moscow/Leningrad, Russia, 1950; Volume 12, p. 582. [Google Scholar]
  20. Kim, C.H.; Nam, S.H.; Lee, S.M. Insecta. (vlll); Ministry of Education: Seoul, Korea, 1982. [Google Scholar]
  21. Schaefer, P.W.; Weseloh, R.M.; Sun, X.L.; Wallner, W.E.; Yan, J.J. Gypsy-moth, Lymantria (=Ocneria) dispar (L.) (Lepidoptera: Lymantriidae), in the People’s Republic of China. Environ. Entomol. 1984, 13, 1535–1541. [Google Scholar] [CrossRef]
  22. Schaefer, P.W.; Ikebe, K.; Higashiura, Y. Gypsy moth, Lymantria dispar (L.) and its natural enemies in the Far East (especially Japan). In Annotated Bibliography and Guide to the Literature through 1986 and Host Plant List for Japan; University of Delaware, Agricultural Experiment Station: Newark, DE, USA, 1988; p. 160. [Google Scholar]
  23. Baranchikov, Y.N. Ecological basis of the evolution of host relationships in Eurasian gypsy moth populations. In Proceedings, Lymantriidae: A Comparison of Features of New and Old World Tussock Moths. GTR-NE-123; U.S. Department of Agriculture, Forest Service, Northeastern Forest Experiment Station: Broomall, PA, USA, 1989; pp. 319–338. [Google Scholar]
  24. Baranchikov, Y.N.; Montgomery, M.E. Tree Suitability for Asian, European and American Populations of Gypsy Moth; General Technical Reports NE-188; USDA Forest Service: Washington, DC, USA, 1994; p. 4. [Google Scholar]
  25. Gninenko, Y.I.; Orlinskii, A.D. Outbreaks of Lymantria dispar in Russian forests during the 1990s. EPPO Bull. 2003, 33, 325–329. [Google Scholar] [CrossRef]
  26. Johns, R.C.; Tobita, H.; Hara, H.; Ozaki, K. Adaptive advantages of dietary mixing different-aged foliage within conifers for a generalist defoliator. Ecol. Res. 2015, 30, 793–802. [Google Scholar] [CrossRef]
  27. Keena, M.A.; Côté, M.J.; Grinberg, P.S.; Wallner, W.E. World distribution of female flight and genetic variation in Lymantria dispar (Lepidoptera: Lymantriidae). Environ. Entomol. 2008, 37, 636–649. [Google Scholar] [CrossRef]
  28. Yang, F.; Luo, Y.; Huang, D.; Cui, X.; Yang, H.; Liu, X.; Shi, J. A preliminary study on flight ability among Chinese populations of Asian gypsy moth, Lymantria dispar. Chin. Agr. Sci. Bull. 2012, 28, 53–57. [Google Scholar]
  29. Bigsby, K.M.; Tobin, P.C.; Sills, E.O. Anthropogenic drivers of gypsy moth spread. Biol. Invasions 2011, 13, 2077. [Google Scholar] [CrossRef]
  30. Walsh, P.J. Asian gypsy moth: The risk to New Zealand. N. Z. For. 1993, 38, 41–43. [Google Scholar]
  31. Schaefer, P.W.; Strothkamp, K.G. Mass flights of Lymantria dispar japonica and Lymantria mathura (Erebidae: Lymantriinae) to commercial lighting, with notes on female viability and fecundity. J. Lepid. Soc. 2014, 68, 124–129. [Google Scholar]
  32. Djoumad, A.; Nisole, A.; Zahiri, R.; Freschi, L.; Picq, S.; Gundersen-Rindal, D.E.; Sparks, M.E.; Dewar, K.; Stewart, D.; Maaroufi, H.; et al. Comparative analysis of mitochondrial genomes of geographic variants of the gypsy moth, Lymantria dispar, reveals a previously undescribed genotypic entity. Sci. Rep. 2017, 7, 14245. [Google Scholar] [CrossRef]
  33. Johnson, D.M.; Liebhold, A.M.; Bjorsnstad, O.N. Geographical variation in periodicity of gypsy moth outbreaks. Ecography 2006, 29, 367–374. [Google Scholar] [CrossRef]
  34. Lindner, M.; Maroschek, M.; Netherer, S.; Kremer, A.; Barbati, A.; Garcia-Gonzalo, J.; Seidl, R.; Delzon, S.; Corona, P.; Kolström, M.; et al. Climate change impacts, adaptive capacity, and vulnerability of European forest ecosystems. For. Ecol. Manag. 2010, 259, 698–709. [Google Scholar] [CrossRef]
  35. Vanhanen, H.; Veteli, T.O.; Päivinen, S.; Kellomäki, S.; Niemela, P. Climate change and range shifts in two insect defoliators: Gypsy moth and nun moth—A model study. Silva Fenn. 2007, 41, 621–638. [Google Scholar] [CrossRef]
  36. Papadopoulou, S.; Chryssochoides, C.; Avtzis, D. Genetic Diversity of Lymantria dispar Linnaeus (Lepidoptera: Lymantriidae) in Northern Greece and Evaluation of the Effectiveness of Novel Insecticides. Biotechnol. Biotechnol. Equip. 2012, 26, 2976–2980. [Google Scholar] [CrossRef]
  37. Wanner, K.W.; Helson, B.V.; Harris, B.J. Laboratory evaluation of two novel strategies to control first-instar gypsy moth larvae with spinosad applied to tree trunks. Pest Manag. Sci. 2002, 58, 817–824. [Google Scholar] [CrossRef] [PubMed]
  38. Dubois, N.R.; Dean, D.H. Synergism between CryIA insecticidal crystal proteins and spores of Bacillus thuringiensis, other bacterial spores, and vegetative cells against Lymantria dispar (Lepidoptera: Lymantriidae) larvae. Environ. Entomol. 1995, 24, 1741–1747. [Google Scholar] [CrossRef]
  39. Georgiev, G.; Hubenov, Z.; Georgieva, M.; Mirchev, P.; Matova, M.; Solter, L.F.; Pilarska, D.; Pilarski, P. Interactions between the introduced fungal pathogen Entomophaga maimaiga and indigenous tachinid parasitoids of gypsy moth Lymantria dispar in Bulgaria. Phytoparasitica 2013, 41, 125–131. [Google Scholar] [CrossRef]
  40. Georgieva, M.; Georgiev, G.; Pilarska, D.; Pilarski, P.; Mirchev, P.; Papazova-Anakieva, I.; Matova, M. First record of Entomophaga maimaiga (Entomophthorales: Entomophthoraceae) in Lymantria dispar populations in Greece and the former yugoslavian republic of Macedonia. Ŝumarski List 2013, 137, 307–311. [Google Scholar]
  41. Papadopoulou, S.; Chryssochoides, C.; Katanos, J. Control of Lymantria dispar L. for eliminating the risk of forage production loss for small ruminants. In Nutritional and Foraging Ecology of Sheep and Goats; Papachristou, T.G., Parissi, Z.M., Ben Salem, H., Morand-Fehr, P., Eds.; CIHEAM: Zaragoza, Spain; FAO: Rome, Italy; NAGREF: Thermi, Greece, 2009; pp. 197–199. [Google Scholar]
  42. Pilarska, D.; McManus, M.; Pilarski, P.; Georgiev, G.; Mirchev, P.; Linde, A. Monitoring the establishment and prevalence of the fungal entomopathogen Entomophaga maimaiga in two Lymantria dispar L. populations in Bulgaria. J. Pest Sci. 2006, 79, 63–67. [Google Scholar] [CrossRef]
  43. Shapiro, M.; McLane, W.; Belli, R. Laboratory evaluation of selected chemicals as antidesiccants for the protection of the entomogenous nematode, Steinernema feltiae (Rhabditidae: Steinernematidae), against Lymantria dispar (Lepidoptera: Lymantriidae). J. Econ. Entomol. 1985, 78, 1437–1441. [Google Scholar] [CrossRef]
  44. Žikić, V.; Stanković, S.S.; Kavallieratos, N.G.; Athanassiou, C.; Grorgiou, P.; Tschorsnig, H.P.; Achterberg, C.V. Parasitoids associated with Lymantria dispar (Lepidoptera: Erebidae) and Malacosoma neustria (Lepidoptera: Lasiocampidae) in Greece and comparative analysis of their parasitoid spectrum in Europe. Zool. Anz. 2017, 270, 166–175. [Google Scholar] [CrossRef]
  45. Zhang, J.; Lapointe, R.; Thumbi, D.; Morin; Lucarotti, C.J. Molecular comparisons of alphabaculovirus-based products: Gypchek with Disparvirus (Lymantria dispar) and TM BioControl-1 with Virtuss (Orgyia pseudotsugata). Can. Entomol. 2010, 142, 546–556. [Google Scholar] [CrossRef]
  46. Harrison, R.L.; Rowley, D.L. Complete genome sequence of the strain of Lymantria dispar multiple nucleopolyhedrovirus found in the gypsy moth biopesticide Virin-ENSh. Genome Announc. 2015, 3, e01407-14. [Google Scholar] [CrossRef]
  47. Hajek, A.E.; van Frankenhuyzen, K. Use of entomopathogens against forest pests. In Microbial Control of Insect and Mite Pests: From Theory to Practice; Lacey, L.A., Ed.; Elsevier: Cambridge, MA, USA, 2017; pp. 313–330. [Google Scholar]
  48. Akhanaev, Y.; Pavlushin, S.; Polenogova, O.; Klementeva, T.; Lebedeva, D.; Okhlopkova, O.; Kolosov, A.; Martemyanov, V. The effect of mixtures of Bacillus thuringiensis-based insecticide and multiple nucleopolyhedrovirus of Lymantria dispar L. in combination with an optical brightener on L. dispar larvae. BioControl 2022, 67, 331–343. [Google Scholar] [CrossRef]
  49. Greathead, D. Parasitoids in classical biological control. In Insect Parasitoids, Proceedings of the 13th Symposium of the Royal Entomological Society of London, Department of Physics Lecture Theatre, Imperial College, London, UK, 18–19 September 1985; Waage, J., Greathead, D., Eds.; London Academic Press: London, UK, 1986; pp. 289–318. [Google Scholar]
  50. Montgomery, M.E.; Wallner, W.E. The Gypsy Moth. In Dynamics of Forest Insect Populations. Population Ecology; Berryman, A.A., Ed.; Springer: Boston, MA, USA, 1988; pp. 353–375. [Google Scholar]
  51. Doane, C.C. Aspects of mating behavior of the gypsy moth. Ann. Entomol. Soc. Am. 1968, 61, 768–773. [Google Scholar] [CrossRef]
  52. Forbush, E.H.; Fernald, C.H. The Gypsy Moth; Wrightand Potter Press: Boston, MA, USA, 1896. [Google Scholar]
  53. Cardé, R.T. Precopulatory sexual behavior of the adult gypsy moth. In The Gypsy Moth: Research toward Integrated Pest Management; Doane, C.C., McManus, M.L., Eds.; USDA Technical Bulletin 1584; USDA: Washington, DC, USA, 1981; pp. 572–587. [Google Scholar]
  54. Charlton, R.E.; Cardé, R.T. Behavioral interactions in the courtship of Lymantria dispar (Lepidoptera: Lymantriidae). Ann. Entomol. Soc. Am. 1990, 83, 89–96. [Google Scholar] [CrossRef]
  55. Timms, L.L.; Smith, S.M. Effects of gypsy moth establishment and dominance in native caterpillar communities of northern oak forests. Can. Entomol. 2011, 143, 479–503. [Google Scholar] [CrossRef]
  56. Campbell, R.W. The analysis of numerical change in gypsy moth populations. For. Sci. 1967, 13, a0001–z0001. [Google Scholar]
  57. Closa, S.; Núñez, L.; Parga, E. Eruga Peluda (Lymantria dispar), L’Insecte Defoliador de les Alzines. Quadern de Natura; Conselleria de Medi Ambien CAIB, Govern de les Illes Balears: Palma, Spain, 2008; p. 26. [Google Scholar]
  58. Junta de Andalucía. Plan de Lucha Integrada Contra la Lagarta Peluda Lymantria dispar (Linnaeus, 1978) en la Comunidad Autónoma de Andalucía; Consejería de Medio Ambiente y Ordenación del Territorio: Seville, Spain, 2013; p. 45. [Google Scholar]
  59. Stefanescu, C.; Soldevila, A.; Gutiérrez, C.; Torre, I.; Ubach, A.; Miralles, M. Explosions demogràfiques de l’eruga peluda del suro, Lymantria dispar (Linnaeus, 1758), als boscos del Montnegre el 2019 i 2020: Possibles causes, impactes i idoneitat dels tractaments per combatre la plaga. Butlletí Inst. Catalana D’història Nat. 2020, 84, 267–279. [Google Scholar]
  60. Leonard, D.E. Diapause in the gypsy moth. J. Econ. Entomol. 1968, 61, 596–598. [Google Scholar] [CrossRef]
  61. Leonard, D.E. Recent developments in ecology and control of the gypsy moth. Ann. Rev. Entomol. 1974, 19, 197–229. [Google Scholar] [CrossRef]
  62. Leonard, D.E. Bioecology of the gypsy moth. Bull. U.S. Dep. Agric. 1981, 1584, 9–29. [Google Scholar]
  63. Grijpma, P. Overview of research on lymantrids in eastern and western Europe. In Proceedings, Lymantriidae: A Comparison of Features of New and Old World Tussock Moth; GTR-NE-123; U.S. Department of Agriculture, Forest Service, Northeastern Forest Experiment Station: Broomall, PA, USA, 1989; pp. 21–49. [Google Scholar]
  64. Sawyer, A.J.; Tauber, M.J.; Tauber, C.A.; Ruberson, J.R. Gypsy moth (Lepidoptera: Lymantriidae) egg development: A simulation analysis of laboratory and field data. Ecol. Model. 1993, 66, 121–155. [Google Scholar] [CrossRef]
  65. Zharkov, D.G.; Tvaradze, M.S. Gypsy moth and its entomophages in the forests of Georgia. In Neparnyy Shelkopryad: Itogi I Perspektivy Issledovaniy; Institut Lesa I Drevesiny SO AN SSSR: Krasnoyarsk, Russia, 1988; p. 22. [Google Scholar]
  66. Ministerio de Agricultura, Pesca y Alimentación. Plagas de Insectos en las Masas Forestales Españolas; Publicaciones del Ministerio de Agricultura, Pesca y Alimentación; Secretaría General Técnica, Servicio de Publicaciones Agrarias: Madrid, Spain, 1981; p. 254. [Google Scholar]
  67. Hernandez-Alonso, R.; Martín-Bernal, E.; Cañada-Martín, J.F.; Pérez-Fortea, V.; Ibarra-Ibáñez, N.; Soriano-Giménez, M. Oruga Defoliadora de las Frondosas, Lymantria dispar L. (Lepidóptero, Fam. Lymantriidae); Informaciones Técnicas 3/2001; Dirección General del Medio Natural, Departamento de Medio Ambiente, Gobierno de Aragón: Zaragoza, Spain, 2001; p. 4. [Google Scholar]
  68. Roonwal, M.L. Structure of the egg-masses and their hairs in some species of Lymantria of importance to forestry (Insecta: Lepidoptera: Lymnantriidae). India For. 1954, 8, 265–276. [Google Scholar]
  69. Katovich, S.; Haack, R. Gypsy moth in the northern hardwood forest. In Northern Hardwood Notes; Hutchinson, J.G., Ed.; U.S. Department of Agriculture, Forest Service, North Central Forest Experiment Station: St. Paul, MN, USA, 1991; Section 7.10. [Google Scholar]
  70. Keena, M.A.; O’Dell, T.M.; Tanner, J.A. Effects of diet ingredient source and preparation method on larval development of laboratory-reared gypsy moth (Lepidoptera, Lymantriidae). Ann. Entomol. Soc. Am. 1995, 88, 672–679. [Google Scholar] [CrossRef]
  71. Gray, D.R. Age-dependent postdiapause development in the gypsy moth (Lepidoptera: Lymantriidae) life stage model. Environ. Entomol. 2009, 38, 18–25. [Google Scholar] [CrossRef] [PubMed]
  72. Gray, D.R.; Ravlin, F.W.; Braine, J.A. Diapause in the gypsy moth: A model of inhibition and development. J. Insect Physiol. 2001, 47, 173–184. [Google Scholar] [CrossRef]
  73. Gray, D.R.; Logan, J.A.; Ravlin, F.W.; Carlson, J.A. Toward a model of gypsy moth egg phenology: Using respiration rates of individual eggs to determine temperature–time requirements of prediapause development. Environ. Entomol. 1991, 20, 1645–1652. [Google Scholar] [CrossRef]
  74. Bell, R.A. Manipulation of diapause in the gypsy moth, Lymantria dispar L., by application of KK-42 and precocious chilling of eggs. J. Insect Physiol. 1996, 42, 557–563. [Google Scholar] [CrossRef]
  75. Giese, R.L.; Cittadino, M.L. Relationship of the Gypsy Moth to the Physical Environment; Staff Paper #6; Department of Forestry, University of Wisconsin-Madison: Madison, WI, USA, 1977; p. 13. [Google Scholar]
  76. Pantyukhov, G.A. The effect of low temperatures on different populations of the brown-tail moth Euproctis chrysorrhoea (L.) and the gypsy moth Lymantria dispar (L.) (Lepidoptera: Orgyidae). Entomol. Rev. 1964, 43, 47–55. [Google Scholar]
  77. Masaki, S. The effect of temperature on the termination of diapause in the egg of Lymantria dispar Linné (Lepidoptera: Lymantriidae). Jpn. J. Appl. Zool. 1956, 21, 148–157. [Google Scholar]
  78. Gray, D.R.; Ravlin, F.W.; Régnière, J.; Logan, J.A. Further advances toward a model of gypsy moth (Lymantria dispar (L.)) egg phenology: Respiration rates and thermal responsiveness during diapause, and age-dependent developmental rates in postdiapause. J. Insect Physiol. 1995, 41, 247–256. [Google Scholar] [CrossRef]
  79. Marr, J.; Director, P.W. Gypsy Moth Monitoring Program; BioForest: Toronto, ON, Canada, 2020. [Google Scholar]
  80. Wanner, K.W.; Helson, B.V.; Harris, B.J. Laboratory and field evaluation of spinosad against the gypsy moth, Lymantria dispar. Pest Manag. Sci. 2000, 56, 855–860. [Google Scholar] [CrossRef]
  81. Weseloh, R.M. Behavioural responses of gypsy moth (Lepidoptera:Lymantridae) larvae to abiotic environmental factors. Environ. Entomol. 1989, 18, 361–367. [Google Scholar] [CrossRef]
  82. Leonard, D.E. Feeding rhythm in larvae of the gypsy moth. J. Econ. Entomol. 1970, 63, 1454–1457. [Google Scholar] [CrossRef]
  83. Campbell, R.W.; Sloan, R.J. Influence of behavioral evolution on gypsy moth pupal survival in sparse populations. Environ. Entomol. 1976, 5, 1211–1217. [Google Scholar] [CrossRef]
  84. Wallner, W.E. Gypsy moth host interactions: A concept of room and board. In Proceedings, Forest Defoliator-Host Interactions: Comparison between Gypsy Moth and Spruce Budworms, New Haven, CT, USA, 5–7 April 1983; General Technical Report, NE-85; Talerico, R.L., Montgomery, M., Eds.; U.S. Department of Agriculture, Forest Service, Northeastern Forest Experiment Station: Broomall, PA, USA, 1983; pp. 5–8. [Google Scholar]
  85. USDA. Gypsy Moth Management in the United States: A Cooperative Approach; Draft Environmental Impact Statement; USDA Forest Service: Washington, DC, USA, 1995. [Google Scholar]
  86. Barbosa, P. Distribution of an endemic level gypsy moth population among various tree species. Environ. Entomol. 1978, 7, 526–527. [Google Scholar] [CrossRef]
  87. Brooks, C.; Hall, D. Gypsy Moth Silvicultural Guidelines for Wisconsin; Wisconsin DNR PUB-FR-123 97; Wisconsin Department of Natural Resources: Madison, WI, USA, 2005; p. 14. [Google Scholar]
  88. Allen, V.T.; Miller, O.F.; Tyler, W.B. Gypsy moth caterpillar dermatitis-revisited. J. Am. Acad. Dermatol. 1991, 24, 979–981. [Google Scholar] [CrossRef]
  89. Leroy, B.M.L.; Lemme, H.; Braumiller, P.; Hilmers, T.; Jacobs, M.; Hochrein, S.; Kienlein, S.; Müller, J.; Pretzsch, H.; Stimm, K.; et al. Relative impacts of gypsy moth outbreaks and insecticide treatments on forest resources and ecosystems: An experimental approach. Ecol. Solut. Evid. 2021, 2, e12045. [Google Scholar] [CrossRef]
  90. Lance, D.R. Host-seeking behavior of the gypsy moth: The influence of polyphagy and highly apparent host plants. In Host-Seeking Behavior and Mechanisms; Herbivorous Insects; Ahmad, S., Ed.; Academic Press: New York, NY, USA, 1983; pp. 210–224. [Google Scholar]
  91. APHIS (Animal and Plant Health Inspection Service). Asian Gypsy Moth. Available online: https://www.aphis.usda.gov/aphis/ourfocus/planthealth/plant-pest-and-disease-programs/pests-and-diseases/gypsy-moth/CT_Gypsy_Moth (accessed on 6 September 2022).
  92. Mosher, F.H. Food plants of the gypsy moth in America. USDA Bull. 1915, 250, 1–39. [Google Scholar]
  93. Shields, V.D.C.; Broomell, B.P.; Salako, J.O.B. Host selection and acceptability of selected tree species by gypsy moth larvae, Lymantria dispar (L.). Ann. Entomol. Soc. Am. 2003, 96, 920–926. [Google Scholar] [CrossRef]
  94. Elkinton, J.S.; Liebhold, A.M. Population dynamics of Gypsy moth in North America. Annu. Rev. Entomol. 1990, 35, 571–596. [Google Scholar] [CrossRef]
  95. Valentine, H.T.; Talerico, R.L. Gypsy moth larval growth and consumption on red oak. For. Sci. 1980, 26, 599–605. [Google Scholar]
  96. Montgomery, M.E. Variation in the susceptibility of tree species for gypsy moth. In Proceedings of the U.S. Department of Agriculture Interagency Gypsy Moth Review 1990, GTR-NE-146, East Windsor, CT, USA, 22–25 January 1990; United States Department of Agriculture, Forest Service, Northeastern Forest Experiment Station: Radnor, PA, USA, 1991; pp. 1–13. [Google Scholar]
  97. Fuester, R.W.; Drea, J.J.; Gruber, F.; Herard, F. Explorations in Europe and Iran by the ARS European Parasite Laboratory: 1972–77. The gypsy moth: Research toward integrated pest management. USDA Tech. Bull. 1981, 1584, 324–340. [Google Scholar]
  98. McManus, M.; Csóka, G. History and impact of gypsy moth in north America and comparison to the recent outbreaks in Europe. Acta Silv. Lignaria Hung. 2007, 3, 47–64. [Google Scholar]
  99. Hirka, A. A 2004. Évi Biotikus És Abiotikus Erdőgazdasági Károk, Valamint a 2005-Ben Várható Károsítások; Hungarian Forest Research Institute: Budapest, Hungary, 2005. [Google Scholar]
  100. Keena, M.A.; Richards, J.Y. Comparison of survival and development of gypsy moth Lymantria dispar L. (Lepidoptera: Erebidae) populations from different geographic areas on North American conifers. Insects 2020, 11, 260. [Google Scholar] [CrossRef] [PubMed]
  101. Lechowicz, M.J.; Mauffette, Y. Host preference of the gypsy moth in eastern North America versus European forests. Rev. Entomol. Que. 1986, 31, 43–51. [Google Scholar]
  102. Rossiter, M. Use of a secondary host by non-outbreak populations of the gypsy moth. Ecology 1987, 68, 857–868. [Google Scholar] [CrossRef]
  103. Strom, B.L.; Hain, F.P.; Ayres, M.P. Field performance of F1-sterile gypsy moth larvae (Lepidoptera: Lymantriidae) on loblolly pine and sweetgum. Environ. Entomol. 1996, 25, 749–756. [Google Scholar] [CrossRef]
  104. Lovett, G.M.; Camja, C.D.; Arthur, M.A.; Weathers, K.C.; Fitzhugh, R.D. Forest ecosystem responses to exotic pests and pathogens in Eastern North America. BioScience 2006, 56, 395–405. [Google Scholar] [CrossRef]
  105. Davidson, C.B.; Johnson, J.E.; Gottschalk, K.W.; Amateis, R.L. Prediction of stand susceptibility and gypsy moth defoliation in Coastal Plain mixed pine hardwoods. Can. J. For. Res. 2001, 31, 1914–1921. [Google Scholar]
  106. Campbell, R.W.; Garlo, A.S. Gypsy moth in New Jersey pine-oak. J. For. 1982, 80, 89–90. [Google Scholar]
  107. Romanyk, N. Les gradations de Lymantria dispar L. en Espagne. Zast. Bilja. 1973, 24, 285–288. [Google Scholar]
  108. Romanyk, N.; Rupérez, A. Principales parásitos observados en los defoliadores de España con atención particular de la Lymantria dispar L. Entomophaga 1960, 5, 229–239. [Google Scholar] [CrossRef]
  109. Leite, R.M.M.R. Ocorrência de Lymantria dispar L. em Pinus radiata D. Don: Estudo do Ciclo de Vida e Comportamento da Praga Neste Hospedeiro: Medidas de Proteção e Combate; Instituto Politécnico de Castelo Branco: Castelo Branco, Portugal, 1993. [Google Scholar]
  110. Miller, J.C.; Hanson, P.E. Laboratory studies on development of gypsy moth, Lymantria dispar (L.) (Lepidoptera: Lymantriidae), larvae on foliage of gymnosperms. Can. Entomol. 1989, 121, 425–429. [Google Scholar] [CrossRef]
  111. Castedo-Dorado, F.; Lago-Parra, G.; Lombardero, M.J.; Liebhold, A.M.; Álvarez-Taboada, M.F. European gypsy moth (Lymantria dispar dispar L.) completes development and defoliates exotic radiata pine plantations in spain. N. Z. J. For. Sci. 2016, 46, 18. [Google Scholar] [CrossRef]
  112. Mead, D.J. Sustainable Management of Pinus Radiata Plantations; FAO: Rome, Italy, 2013. [Google Scholar]
  113. Aber, R.; De Melfi, T.; Gill, T.; Healey, B.; McCarthy, M.A. Rash illnesses associated with gypsy moth caterpillars, Pennsylvania. Morb. Mortal. Wkly. Rep. 1982, 31, 169–170. [Google Scholar]
  114. Liebhold, A.M.; Mastro, V.; Schaefer, P.W. Learning from the legacy of Léopold Trouvelot. Bull. Entomol. Soc. Am. 1989, 35, 20–22. [Google Scholar] [CrossRef]
  115. Diaz, J.H. The Evolving Global Epidemiology, Syndromic Classification, Management, and Prevention of Caterpillar Envenoming. Am. J. Trop. Med. Hyg. 2005, 72, 347–357. [Google Scholar] [CrossRef]
  116. Wu, Y.; Molongoski, J.J.; Winograd, D.F.; Bogdanowicz, S.M.; Louyakis, A.S.; Lance, D.R.; Mastro, V.C.; Harrison, R.G. Genetic structure, admixture and invasion success in a Holarctic defoliator, the gypsy moth (Lymantria dispar, Lepidoptera: Erebidae). Mol. Ecol. 2015, 24, 1275–1291. [Google Scholar] [CrossRef]
  117. Glare, T.R.; Walsh, P.J.; Kay, M.; Barlow, N.D. Strategies for the Eradication or Control of Gypsy Moth in New Zealand; Lincoln, Agresearch: Lincoln, New Zealand, 2003; pp. 30–31. [Google Scholar]
  118. Wulf, A.; Graser, E. Gypsy moth outbreaks in Germany and neighboring countries. Nachr. Dtsch. Pflanzenschutzd. 1996, 48, 265–269. [Google Scholar]
  119. Grayson, K.L.; Johnson, D.M. Novel insights on population and range edge dynamics using an unparalleled spatiotemporal record of species invasion. J. Anim. Ecol. 2018, 87, 581–593. [Google Scholar] [CrossRef]
  120. Tobin, P.C.; Robinet, C.; Johnson, D.M.; Whitmire, S.L.; Bjornstad, O.N.; Liebhold, A.M. The role of Allee effects in gypsy moth, Lymantria dispar (L.), invasions. Popul. Ecol. 2009, 51, 373–384. [Google Scholar] [CrossRef]
  121. Aukema, J.E.; Leung, B.; Kovacs, K.; Chivers, C.; Britton, K.O.; Englin, J.; Frankel, S.J.; Haight, R.G.; Holmes, T.P.; Liebhold, A.M.; et al. Economic impacts of non-native forest insects in the continental United States. PLoS ONE 2011, 6, e24587. [Google Scholar] [CrossRef]
  122. Morin, R.S.; Liebhold, A.M. Invasive forest defoliator contributes to the impending downward trend of oak dominance in eastern North America. Forestry 2016, 89, 284–289. [Google Scholar] [CrossRef]
  123. McNamara, D.G. EPPO’s perspective on the gypsy moth in Europe. In Proceedings of the 1995 Annual Gypsy Moth Review, Traverse City, MI, USA, 5–8 November 1995; Michigan Department of Agriculture: Lansing, MI, USA, 1995; pp. 60–65. [Google Scholar]
  124. Keena, M.A.; Grinberg, P.S.; Wallner, W.E. Inheritance of female flight in Lymantria dispar (Lepidoptera: Lymantriidae). Environ. Entomol. 2007, 36, 484. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  125. Tobin, P.C.; Bai, B.B.; Eggen, D.A.; Leonard, D.S. The ecology, geopolitics, and economics of managing Lymantria dispar in the United States. Int. J. Pest Manag. 2012, 58, 195–210. [Google Scholar] [CrossRef]
  126. Weseloh, R.M. Evidence for limited dispersal of larval gypsy moth, Lymantria dispar L. (Lepidoptera: Lymantriidae). Can. Entomol. 1997, 129, 355–361. [Google Scholar] [CrossRef]
  127. Campbell, R.W. Population dynamics. In The Gypsy Moth: Research toward Integrated Pest Management; USDA Forest Service Technical Bulletin 1584; Government Printing Office: Washington, DC, USA, 1981; pp. 65–214. [Google Scholar]
  128. Lance, D.R.; Barbosa, P. Host tree influences on the dispersal of late instar gypsy moths, Lymantria dispar. Oikos 1982, 38, 1–7. [Google Scholar] [CrossRef]
  129. Deml, R.; Dettner, J.K. “Balloon hairs” of gypsy moth larvae (Lepidoptera: Lymantriidae): Morphology and comparative chemistry. Comp. Biochem. Physical. 1995, 112B, 673–681. [Google Scholar] [CrossRef]
  130. McManus, M.L. The Role of Behavior in the Disperal of Newly Hatch Gypsy Moth Larvae; Research Paper NE-267; USDA Forest Service, Northeastern Forest Experiment Station: Upper Darby, PA, USA, 1973. [Google Scholar]
  131. Liebhold, A.M.; Halverson, J.A.; Elmes, G.A. Gypsy moth invasion in North America: A quantitative analysis. J. Biogeogr. 1992, 19, 513–520. [Google Scholar] [CrossRef]
  132. McFadden, M.W.; McManus, M.E. An insect out of control? The potential for spread and establishment of the gypsy moth in new forest areas in the United States. In Insect Guilds: Patterns of Interaction with Host Trees; Baranchikov, Y.N., Mattson, W.J., Hain, F.P., Payne, T.L., Eds.; USDA Forest Service, Northeastern Forest Experiment Station: Radnor, PA, USA, 1991; pp. 172–186. [Google Scholar]
  133. Kearns, D.N.; Tobin, P.C. Oregon vs. the gypsy moth: Forty years of battling an invasive species. Am. Entomol. 2020, 66, 50–58. [Google Scholar] [CrossRef]
  134. Tobin, P.; Blackburn, L.M. Slow the Spread: A National Program to Manage the Gyspy Moth; General Technical Reports NRS-6; US Department of Agriculture, Forest Service, Northern Research Station: Newton Square, PA, USA, 2007. [Google Scholar]
  135. Picq, S.; Keena, M.; Havill, N.; Stewart, D.; Pouliot, E.; Boyle, B.; Levesque, R.C.; Hamelin, R.C.; Cusson, M. Assessing the potential of genotyping-by-sequencing-derived single nucleotide polymorphisms to identify the geographic origins of intercepted gypsy moth (Lymantria dispar) specimens: A proof-of-concept study. Evol. Appl. 2018, 11, 325–339. [Google Scholar] [CrossRef]
  136. Gray, D.R. The gypsy moth life stage model: Landscapewide estimates of gypsy moth establishment using a multigenerational phenology model. Ecol. Model. 2004, 176, 155–171. [Google Scholar] [CrossRef]
  137. Tobin, P.C.; Gray, D.R.; Liebhold, A.M. Supraoptimal temperatures influence the range dynamics of a non-native insect. Divers. Distrib. 2014, 20, 813–823. [Google Scholar] [CrossRef]
  138. Tobin, P.C.; Kean, J.M.; Suckling, D.M.; McCullough, D.G.; Herms, D.A.; Stringer, L.D. Determinants of successful arthropod eradication programs. Biol. Invasions 2014, 16, 401–414. [Google Scholar] [CrossRef]
  139. Contarini, M.; Onufrieva, K.S.; Thorpe, K.W.; Raffa, K.F.; Tobin, P.C. Mate-finding failure as an important cause of Allee effects along the leading edge of an invading insect population. Entomol. Exp. Appl. 2009, 133, 307–314. [Google Scholar] [CrossRef]
  140. Yamanaka, T.; Liebhold, A.M. Mate-location failure, the Allee effect, and the establishment of invading populations. Popul. Ecol. 2009, 51, 337–340. [Google Scholar] [CrossRef]
  141. Rhainds, M. Size-dependent realized fecundity in two lepidopteran capital breeders. Environ. Entomol. 2015, 44, 1193–1200. [Google Scholar] [CrossRef]
  142. Cloyd, R.A.; Nixon, P.L.; Gypsy Moth. University of Illinois Extension. Available online: https://extension.illinois.edu/gypsymoth/biology.cfm (accessed on 6 September 2022).
  143. Myers, J.H.; Cory, J.S. Population Cycles in Forest Lepidoptera Revisited. Annu. Rev. Ecol. Evol. Syst. 2013, 44, 565–592. [Google Scholar] [CrossRef]
  144. Roy, A.S.; McNamara, D.G.; Smith, I.M. Situation of Lymantria dispar in Europe. EPPO Bull. 1995, 25, 611–616. [Google Scholar] [CrossRef]
  145. Ananko, G.G.; Kolosov, A.V. Asian gypsy moth (Lymantria dispar L.) populations: Tolerance of eggs to extreme winter temperatures. J. Therm. Biol. 2021, 102, 103123. [Google Scholar] [CrossRef]
  146. Elton, C.S. Periodic fluctuations in the numbers of animals: Their causes and effects. Br. J. Exp. Biol. 1924, 2, 119–163. [Google Scholar] [CrossRef]
  147. Johnson, D.M.; Liebhold, A.M.; Bjornstad, O.N.; Mcmanus, M.L. Circumpolar variation in periodicity and synchrony among gypsy moth populations. J. Anim. Ecol. 2005, 74, 882–892. [Google Scholar] [CrossRef]
  148. Hlasny, T.; Trombik, J.; Holusa, J.; Lukasova, K.; Grendar, M.; Turcani, M.; Zubrik, M.; Tabakovic-Tosic, M.; Hirka, A.; Buksha, I.; et al. Multi-decade patterns of gypsy moth fluctuations in the Carpathian Mountains and options for outbreak forecasting. J. Pest Sci. 2016, 89, 413–425. [Google Scholar] [CrossRef]
  149. Lovett, G.M.; Christenson, L.M.; Groffman, P.M.; Jones, C.G.; Hart, J.E.; Mitchell, M.J. Insect defoliation and nitrogen cycling in forests. BioScience 2002, 52, 335–341. [Google Scholar] [CrossRef] [Green Version]
  150. Kosola, K.R.; Durall, D.M.; Robertson, G.P.; Dickmann, D.I.; Parry, D.; Russell, C.A.; Paul, E.A. Resilience of mycorrhizal fungi on defoliated and fertilized hybrid poplars. Can. J. Bot. 2004, 82, 671–680. [Google Scholar] [CrossRef]
  151. Campbell, R.W.; Sloan, R.J. Forest stand responsesto defoliation by the gypsy moth. For. Sci. 1977, 19, 1–34. [Google Scholar]
  152. Gottschalk, K.W. Gypsy moth effects on mast production. In Proceedings of the Workshop: Southern Appalachian Mast Management, Knoxville, TN, USA, 14–16 August 1989; McGee, C.E., Ed.; University of Tennessee: Knoxville, TN, USA, 1990; pp. 42–50. [Google Scholar]
  153. Wu, Y.; Bogdanowicz, S.M.; Andres, J.A.; Vieira, K.A.; Wang, B.; Cossé, A.; Pfister, S.E. Tracking invasions of a destructive defoliator, the gypsy moth (Erebidae: Lymantria dispar): Population structure, origin of intercepted specimens, and Asian introgression into North America. Evol. Appl. 2020, 13, 2056–2070. [Google Scholar] [CrossRef]
  154. McCullough, D.M.; Bauer, L.S. Bt: One Option for Gypsy Moth Management; Ext. Bull. E-2724; Michigan State University Extension: East Lansing, MI, USA, 2000; p. 4. [Google Scholar]
  155. Bradshaw, C.J.A.; Leroy, B.; Bellard, C.; Roiz, D.; Albert, C.; Fournier, A.; Barbet-Massin, M.; Salles, J.M.; Simard, F.; Courchamp, F. Massive yet grossly underestimated global costs of invasive insects. Nat. Commun. 2016, 7, 12986. [Google Scholar] [CrossRef]
  156. Harrison, R.L.; Rowley, D.L.; Keena, M.A. Pathology and genome sequence of a Lymantria dispar multiple nucleopolyhedrovirus (LdMNPV) isolate from Heilongjiang, China. J. Invertebr. Pathol. 2020, 177, 107495. [Google Scholar] [CrossRef]
  157. Gottschalk, K.W. Silvicultural Guidelines for Forest Stands Threatened by the Gypsy Moth; GTR NE-171; Department of Agriculture Forest Service Northeastern Forest Experiment Station: Radnor, PA, USA, 1993. [Google Scholar]
  158. Schwenke, W. Die Forstschädlinge Europas, Ein Handbuch in Fünf Bäden. Autorenkollektiv: Band 3. Schmetterlinge, 1st ed.; Paul Parey: Hamburg/Berlin, Germany, 1978; p. 467. [Google Scholar]
  159. Keremidchiev, M.T. Dynamics of outbreaks of the gypsy moth (Lymantria dispar L.) in the People’s Republic of Bulgaria. In Proceedings of the 13th International Congres of Entomology, Moscow, Russia, 2–9 August 1968; Bei-Bienko, G.Y., Ed.; Volume 3, pp. 51–54. [Google Scholar]
  160. Milenković, M.; Ducić, V. The solar activity cycles and the outbreaks of the Gypsy Moth—Lymantria dispar L. (Lepidoptera: Lymantriidae) in Serbia. Ecol. Montenegrina 2016, 7, 538–545. [Google Scholar] [CrossRef]
  161. Živojinović, S. Introduction. Gypsy-moth-Results of the activity on its study and control in our country in the course of 1957. Zast. Bilja 1957, 52/53, 3–6. [Google Scholar]
  162. Lipa, J.J.; Kolk, A. The recent situation of the gypsy moth (Lymantria dispar) and other Lymantariids in Poland. Bull. OEPP 1995, 25, 623–629. [Google Scholar] [CrossRef]
  163. Landmann, G.; Barthod, C. La santé des forêts françaises en 1994. Rev. For. Française 1996, 48, 101. [Google Scholar] [CrossRef]
  164. Krehan, H. Schwammspinner-Bekämpfung: Ist sie in Österreich möglich, ist sie notwendig? Forstsch. Aktuell 1994, 15, 13. [Google Scholar]
  165. Anon. PBMD Bulletin Forstschutz-Überblick 1994; Eidgenössische Forschungsanstalt für Wald, Schnee und Landschaft: Birmensdorf, Switzerland, 1995. [Google Scholar]
  166. Cannon, R.J.C.; Koerper, D.; Ashby, S.; Baker, R.; Bartlett, P.W.; Brookes, G.; Burgess, R.; Cheek, S.; Evans, H.F.; Hammon, R.; et al. Gypsy moth, Lymantria dispar, outbreak in Northeast London, 1995–2003. Int. J. Pest. Sci. 2004, 50, 259–273. [Google Scholar] [CrossRef]
  167. Kailidis, D.S. Forest Entomology and Zoology, 4th ed.; Christodoulidis Press: Thessaloniki, Greece, 1991; p. 536. [Google Scholar]
  168. Blanch Rissech, F.; Massana Ribas, R.M. Les industries sureres a Llagostera. Crònica 1992, 6, 1–12. [Google Scholar]
  169. Soldevila, A. Causes de les Explosions Demogràfiques i Mètodes de Seguiment de la Papallona Lymantria dispar Als Boscos del Montnegre. Bachelor Thesis, University of Girona, Girona, Spain, 2020. [Google Scholar]
  170. Tardà, A.; Corbera, J.; Riera, R. Estudi de L’àrea D’afectació de L’eruga Peluda del Suro al Massís del Montnegre a Partir D’imatges Sentinel-2; Institut Cartogràfic i Geològic de Catalunya i Diputació de Barcelona: Generalitat de Catalunya, Spain, 2021; p. 18. [Google Scholar]
  171. Kurenshchikov, D.K.; Martemyanov, V.V.; Imranova, E.L. Features of the far eastern gypsy moth (Lymantria dispar L.) population outbreak. Contemp. Probl. Ecol. 2020, 13, 172–179. [Google Scholar] [CrossRef]
  172. Shamuratova, N.G. Gypsy moth (Lymantria dispar L.) population in Uzbekistan and pathogenicity of the nuclear polyhedrosis virus. Eur. Sci. Rev. 2018, 11, 204–206. [Google Scholar]
  173. Kozhevnikova, L.N.; Levykh, A.Y.; Panchenko, V.Y. Distribution of Lymantria dispar in forests of CSI «Kyzylzharskoe forestry» of the North Kazakhstan region. Karaganda Univ. Bull. Ser. Biomed. Geogr. 2018, 91, 33–39. [Google Scholar]
  174. Krcmar-Nozic, E.; Wilson, B.; Arthur, L. The Potential Impacts of Exotic Forest Pests in North America: A Synthesis of Research; Pacific Forestry Centre: Victoria, BC, Canada, 2000; pp. 12–13. [Google Scholar]
  175. Pernek. M.; Pilaš. I.; Vrbek. B.; Benko. M.; Hrašovec. B.; Milković. J. Forecasting the impact of the gypsy moth on lowland hardwood forests by analyzing the cyclical pattern of population and climate data series. For. Ecol. Manag. 2008, 255, 1740–1748. [Google Scholar] [CrossRef]
  176. Zhang, J.; Cong, Q.; Rex, E.A.; Hallwachs, W.; Janzen, D.H.; Grishin, N.V.; Gammon, D.B. Gypsy moth genome provides insights into flight capability and virus–host interactions. Proc. Natl. Acad. Sci. USA 2019, 116, 1669–1678. [Google Scholar] [CrossRef]
  177. Smitley, D.R.; Davis, T.W. Aerial application of Bacillus thuringiensis for suppression of gypsy moth (Lepidoptera: Lymantriidae) in Populus–Quercus forests. J. Econ. Entomol. 1993, 86, 1178–1184. [Google Scholar] [CrossRef]
  178. Luciano, P.; Lentini, A. Ten years of microbiological control program against lepidopterous defoliators in Sardinian cork oak forests. IOBC/WPRS Bull. 2012, 76, 175–178. [Google Scholar]
  179. Tobin, P.C.; Whitmire, S.L. Spread of gypsy moth (Lepidoptera: Lymantriidae) and its relationship to defoliation. Environ. Entomol. 2005, 34, 1448–1455. [Google Scholar] [CrossRef]
  180. Tobin, P.C.; Liebhold, A.M.; Roberts, E.A.; Blackburn, L.M. Estimating Spread Rates of Non-native Species: The Gypsy Moth as a Case Study. In Invasive Alien Species: Pest Risk Modelling and Mapping; Venette, R.C., Ed.; CABI: Wallingford, UK, 2015; pp. 131–144. [Google Scholar]
  181. Onufrieva, K.S.; Hickman, A.D.; Leonard, D.S.; Tobin, P.C. Relationship between efficacy of mating disruption and gypsy moth density. Int. J. Pest Manag. 2019, 65, 44–52. [Google Scholar] [CrossRef]
  182. Luciano, P.; Prota, R. La dinamica di popolazione di Lymantria dispar L. in Sardegna. Indicatori della gradazione ricavati dale ovideposizioni. Studi Sassar. III 1981, 27, 137–160. [Google Scholar]
  183. Luciano, P.; Prota, R. Osservazioni sulla densità di popolazione di Lymantria dispar L. nelle principali aree subericole della Sardegna. Studi Sassar. III 1982, 28, 168–179. [Google Scholar]
  184. Mannu, R.; Olivieri, M.; Cocco, A.; Lentini, A. Development of Enumerative and Binomial Sequential Sampling Plans for Monitoring Lymantria dispar (L.) (Lepidoptera Erebidae) in Mediterranean Oak Forests. Agronomy 2022, 12, 1501. [Google Scholar] [CrossRef]
  185. Herms, D.A. Assessing management options for gypsy moth. Pestic. Outlook 2003, 14, 14–18. [Google Scholar] [CrossRef]
  186. Kumar, S. Biopesticides: A need for food and environmental safety. J. Biofertil. Biopestic. 2012, 3, e107. [Google Scholar] [CrossRef]
  187. Nicolopoulou-Stamati, P.; Maipas, S.; Kotampasi, C.; Stamatis, P.; Hens, L. Chemical pesticides and human health: The urgent need for a new concept in agriculture. Front. Public Health 2016, 4, 148. [Google Scholar] [CrossRef]
  188. Rausell, C.; Martinez-Ramirez, A.C.; Garcia Roblez, I.; Real, M.D. The toxicity and physiological effects of Bacillus thuringiensis toxins and formulations on Thaumetopoea pityocampa, the pine processionary caterpillar. Pestic. Biochem. Physiol. 1999, 65, 44–54. [Google Scholar] [CrossRef]
  189. Kalender, Y.; Uzunhisarcikli, M.; Ogutcu, A.; Suludere, Z.; Kalender, S. Effects of endosulfan on Thaumetopoea pityocampa (Lepidoptera: Thaumetopoeidae) larvae. Folia Biol. 2005, 53, 3–4. [Google Scholar] [CrossRef]
  190. Ogutcu, A.; Suludere, Z.; Uzunhisarcikli, M.; Kalender, Y. Effects of Bacillus thuringiensis kurstaki on Malpighian tubule cells of Thaumetopoea pityocampa (Lepidoptera: Thaumetopoeidae) larvae. Folia Biol. 2005, 53, 7–11. [Google Scholar] [CrossRef]
  191. Aslanturk, A.; Kalender, S.; Uzunhisarcikli, M.; Kalender, Y. Effects of methidathion on antioxidant enzyme activities and malondialdehyde level in midgut tissues of Lymantria dispar (lepidoptera) larvae. J. Entomol. Res. Soc. 2011, 13, 27–38. [Google Scholar]
  192. Liebhold, A.; McManus, M. The evolving use of insecticides in gypsy moth management. J. For. 1999, 97, 20–23. [Google Scholar]
  193. Sharov, A.A.; Leonard, D.; Liebhold, A.M.; Clemens, N.S. Evaluation of preventive treatments in low-density gypsy moth populations. J. Econ. Entomol. 2002, 95, 1205–1215. [Google Scholar] [CrossRef]
  194. Jones, C.G.; Ostfeld, R.S.; Richard, M.P.; Schauber, E.M.; Wolff, J.O. Chain reactions linking acorns to gypsy moth outbreaks and Lyme disease. Science 1998, 279, 1023–1026. [Google Scholar] [CrossRef]
  195. Bess, H.A. Population ecology of the gypsy moth Porthetria dispar L. (Lepidoptera: Lymantriidae). Conn. Agric. Exp. Stn. Bull. 1961, 646, 1–43. [Google Scholar]
  196. Weseloh, R.M. Changes in population size, dispersal behaviour, and reproduction of Calosoma sycophanta (Coleoptera: Carabidae), associated with changes in gypsy moth, Lymantria dispar (Lepidoptera: Lymantriidae), abundance. Environ. Entomol. 1985, 14, 370–377. [Google Scholar] [CrossRef]
  197. Weseloh, R.M. Predation by Calosoma sycophanta L (Coleoptera, Carabidae) evidence for a large impact on gypsy moth Lymantria dispar pupae. Can. Entomol. 1985, 117, 1117–1126. [Google Scholar] [CrossRef]
  198. Burgess, A.F.; Crossman, S.S. Imported Insect Enemies of the Gypsy Moth and the Browntail Moth; USDA Technical Bulletin 86; USDA: Washington, DC, USA, 1929. [Google Scholar]
  199. Hoch, G.; Kahlbacher, G.; Schopf, A. Gypsy moth revisited: Studies on the natural enemy complex of Lymantria dispar L. (Lep., Lymantriidae) during an outbreak in a well known gypsy moth area. Mitt. Dtsch. Ges. Allg. Angew. Entomol. 2006, 15, 201–204. [Google Scholar]
  200. Kryzhanovsky, O.L. Calosoma sycophanta. In Areas of Insects in the European Part of the USSR; Gorodkov, K.B., Ed.; Atlas: Leningrad, Russia, 1981; p. 20. [Google Scholar]
  201. Kryzhanovsky, O.L.; Belousov, I.A.; Kabak, I.I.; Kataev, B.M.; Makarov, K.V.; Shilenkov, V.G. A Checklist of the Ground-Beetles of Russia and Adjacent Lands (Insecta, Coleoptera, Carabidae); Pensoft Publishers: Moscow, Russia, 1995; p. 271. [Google Scholar]
  202. Kryzhanovsky, O.L.; Obydov, D.V. Krasotel Pakhuchiy Calosoma sycophanta; Red Data Book of the Russian Federation: Moscow, Russia, 2001; p. 122. [Google Scholar]
  203. Bespalov, A.N.; Dudko, R.Y.; Lyubechanskii, I.I. Additions to the ground beetle fauna (Coleoptera, Carabidae) of the Novosibirsk Oblast: Do the southern species spread to the north? Evraziatskii Entomol. Zhurnal 2010, 9, 625–628. [Google Scholar]
  204. Ostfeld, R.S.; Jones, C.G.; Wolff, J.O. Of mice and mast: Ecological connections in eastern deciduous forests. BioScience 1996, 46, 323–330. [Google Scholar] [CrossRef]
  205. Gschwantner, T.; Hoch, G.; Schopf, A. Impact of predators on artificially augmented populations of Lymantria dispar L. Pupae (Lep., Lymantriidae). J. Appl. Entomol. 2002, 126, 66–73. [Google Scholar] [CrossRef]
  206. Liebhold, A.M.; Higashiura, Y.; Unno, A. Forest type affects predation on gypsy moth (Lepidoptera: Lymantriidae) pupae in Japan. Environ. Entomol. 1998, 27, 858–862. [Google Scholar] [CrossRef]
  207. Liebhold, A.M.; Raffa, K.F.; Diss, A.L. Forest type affects predation on gypsy moth pupae. Agric. For. Entomol. 2005, 7, 179–185. [Google Scholar] [CrossRef]
  208. Turcani, M.; Novotny, J.; Zubrik, M.; McManus, M.L.; Pilarksa, D.; Maddox, J. The role of biotic factors in gypsy moth population dynamics in Slovakia: Present knowledge. In Proceedings of the Integrated Management and Dynamics of Forest Defoliating Insects, Victoria, BC, Canada, 15–19 August 1999; Liebhold, A.M., McManus, M.L., Otvos, I.S., Fosbroke, S.L.C., Eds.; General Technical Reports NE-277. USDA Forest Service, Northeastern Research Station: Newtown Square, PA, USA, 2001; pp. 152–167. [Google Scholar]
  209. Reichart, G. Birds destroying eggs of Lymantria dispar L. Aquila 1959, 77, 315–317. [Google Scholar]
  210. Higashiura, Y. Survival of eggs in the gypsy-moth Lymantria dispar L. Predation by birds. J. Anim. Ecol. 1989, 58, 403–412. [Google Scholar] [CrossRef]
  211. Turcani, M.; Liebhold, A.; McManus, M.; Novotny, J. Preliminary results on predation of gypsy moth egg masses in Slovakia. In Proceedings of the Ecology, Survey and Management of Forest Insects, Kraków, Poland, 1–5 September 2002; McManus, M.L., Liebhold, A.M., Eds.; General Technical Reports NE-311. USDA Forest Service, Northeastern Research Station: Newtown Square, PA, USA, 2002; pp. 115–120. [Google Scholar]
  212. Cooper, R.J.; Smith, H.R. Predation on gypsy-moth (Lepidoptera, Lymantriidae) egg masses by birds. Environ. Entomol. 1995, 24, 571–575. [Google Scholar] [CrossRef]
  213. Weseloh, R.M. Behaviour of the gypsy-moth predator, Calosoma sycophanta L (Carabidae, coleoptera), as influenced by time of day and reproductive status. Can. Entomol. 1993, 125, 887–894. [Google Scholar] [CrossRef]
  214. Weseloh, R.; Bernon, G.; Butler, L.; Fuester, R.; McCullough, D.; Stehr, F. Releases of Calosoma sycophanta (Coleoptera: Carabidae) near the edge of gypsy moth (Lepidoptera: Lymantriidae) distribution. Environ. Entomol. 1995, 24, 1713–1717. [Google Scholar] [CrossRef]
  215. Burgess, A.F. Calosoma sycophanta: Its life history, behavior, and successful colonization in New England. Bull. U.S. Dep. Agric. 1911, 101, 1–94. [Google Scholar]
  216. Evans, A.V. The forest caterpillar hunter, Calosoma sycophanta, an Old World species confirmed as part of the Virginia beetle fauna (Coleoptera: Carabidae). Banisteria 2009, 34, 33–37. [Google Scholar]
  217. Goertz, D.; Hoch, G. Influence of the forest caterpillar hunter Calosoma sycophanta on the transmission of microsporidia in larvae of the gypsy moth Lymantria dispar. Agric. For. Entomol. 2013, 15, 178–186. [Google Scholar] [CrossRef]
  218. Howard, L.O.; Fiske, W.F. The importation into the United States of the parasites of the gypsy moth and brown-tailed moth. Bull. U.S. Dep. Agric. 1911, 91, 312. [Google Scholar]
  219. Hoy, M.A. Establishment of gypsy moth parasitoids in North America: An evaluation of possible reasons for establishment or non-establishment. In Perspectives in Forest Entomology; Anderson, J.F., Kaya, H.K., Eds.; Academic Press: New York, NY, USA, 1976; pp. 215–232. [Google Scholar]
  220. Reardon, R.C. Parasite incidence and ecological relationships in field populations of gypsy moth Lepidoptera-Lymantriidae larvae and pupae. Environ. Entomol. 1976, 5, 981–987. [Google Scholar] [CrossRef]
  221. Glare, T.R.; Barlow, N.D.; Walsh, P.J. Potential agents for eradication or control of gypsy moth in New Zealand. In Proceedings of the New Zealand Plant Protection Conference, Hamilton, New Zealand, 12 August 1998; pp. 224–229. [Google Scholar]
  222. Webb, R.E.; Peiffer, R.; Fuester, R.W.; Thorpe, K.W.; Calabrese, L.; McLaughlin, J.M. An evaluation of the residual activity of traditional, safe, and biological insecticides against the gypsy moth. J. Arboric. 1998, 24, 286–293. [Google Scholar] [CrossRef]
  223. Martin, J.C.; Bonneau, X. Bacillus thuringiensis 30 ans de lutte contre les chenilles defoliatrices en foret. Phytoma Défense Végétaux 2006, 590, 4–7. [Google Scholar]
  224. Crickmore, N. Beyond the spore—Past and future developments of Bacillus thuringiensis as a biopesticide. J. Appl. Microbiol. 2006, 101, 616–619. [Google Scholar] [CrossRef]
  225. Mannu, R.; Cocco, A.; Luciano, P.; Lentini, A. Influence of Bacillus thuringiensis application timing on population dynamics of gypsy moth in Mediterranean cork oak forests. Pest Manag. Sci. 2020, 76, 1103–1111. [Google Scholar] [CrossRef]
  226. Scriber, J.M. Non-target impacts of forest defoliator management options: Decision for no spraying may have worse impacts on non-target Lepidoptera than Bacillus thuringiensis insecticides. J. Insect Conserv. 2004, 8, 243–263. [Google Scholar] [CrossRef]
  227. Bateman, R. Application of Biopesticides. In Pesticide Application Methods, 4th ed.; Matthews, G.A., Bateman, R., Miller, P., Eds.; John Wiley & Sons: Oxford, UK, 2014; pp. 411–427. [Google Scholar]
  228. Reardon, R.C.; Podgwaite, J.D. Summary of efficacy evaluations using aerially applied Gypchek® against gypsy moth in the U.S.A. Environ. Sci. Health 1994, B29, 739–756. [Google Scholar] [CrossRef]
  229. Lentini, A.; Mannu, R.; Cocco, A.; Ruiu Pino, A.; Cerboneschi, A.; Luciano, P. Long-term monitoring and microbiological control programs against lepidopteran defoliators in the cork oak forests of Sardinia (Italy). Ann. Silvic. Res. 2019, 45, 21–30. [Google Scholar]
  230. Glare, T.R.; O’Callaghan, M. Bacillus thuringiensis: Biology, Ecology and Safety; John Wiley & Sons: New York, NY, USA, 2000. [Google Scholar]
  231. Maczuga, S.A.; Mierzejewski, K.J. Droplet size and density effects of Bacillus thuringiensis kurstaki on gypsy moth (Lepidoptera: Lymantriidae) larvae. J. Econ. Entomol. 1995, 88, 1376–1379. [Google Scholar] [CrossRef]
  232. Speare, A.T.; Colley, R.H. 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 and Potter Printing Co.: Boston, MA, USA, 1912. [Google Scholar]
  233. Andreadis, T.G.; Weseloh, R.M. Discovery of Entomophaga maimaiga in North American gypsy moth, Lymantria dispar. Proc. Natl. Acad. Sci. USA 1990, 87, 2461–2465. [Google Scholar] [CrossRef]
  234. Hajek, A.E.; Humber, R.A.; Griggs, M.H. Decline in virulence of Entomophaga maimaiga (Zygomycetes: Entomophthorales) with repeated in vitro subculture. J. Invertebr. Pathol. 1990, 56, 91–97. [Google Scholar] [CrossRef]
  235. Nielsen, C.; Milgroom, M.G.; Hajek, A.E. Genetic diversity in the gypsy moth fungal pathogen Entomophaga maimaiga from founder populations in North America and source populations in Asia. Mycol. Res. 2005, 109, 941–950. [Google Scholar] [CrossRef]
  236. Pilarska, D.; McManus, M.; Hajek, A.; Herard, F.; Vega, F.; Pilarski, P.; Markova, G. Introduction of the entomopathogenic fungus Entomophaga maimaiga Hum., Shim. & Sop. (Zygomycetes: Entomophtorales) to a Lymantria dispar (L.) (Lepidoptera: Lymantriidae) population in Bulgaria. J. Pest Sci. 2000, 73, 125–126. [Google Scholar]
  237. Zúbrik, M.; Hajek, A.; Pilarska, D.; Spilda, I.; Georgiev, G.; Hrasovec, B.; Hirka, A.; Goertz, D.; Hoch, G.; Barta, M.; et al. The potential for Entomophaga maimaiga to regulate gypsy moth Lymantria dispar (L.) (Lepidoptera: Erebidae) in Europe. J. Appl. Entomol. 2016, 140, 565–579. [Google Scholar] [CrossRef]
  238. Zúbrik, M.; Barta, M.; Pilarska, D.; Goertz, D.; Úradník, M.; Galko, J.; Vakula, J.; Gubka, A.; Rell, S.; Kunca, A. First record of Entomophaga maimaiga (Entomophthorales: Entomophthoraceae) in Slovakia. Biocontrol Sci. Technol. 2014, 24, 710–714. [Google Scholar] [CrossRef]
  239. Tabaković-Tošić, M.; Georgiev, G.; Mirchev, P.; Tošić, D.; Golubović-Ćurguz, V. Entomophaga maimaiga—New entomopathogenic fungus in the Republic of Serbia. Afr. J. Biotechnol. 2012, 34, 8571–8577. [Google Scholar] [CrossRef]
  240. Tabaković-Tošić, M.; Georgieva, M.; Hubenov, Z.; Georgiev, G. Impact of tachinid parasitoids of gypsy moth (Lymantria dispar) after the natural spreading and introduction of fungal pathogen Entomophaga maimaiga in Serbia. J. Entomol. Zool. Stud. 2014, 2, 262–266. [Google Scholar]
  241. Cory, J.S.; Myers, J.H. The ecology and evolution of insect baculoviruses. Annu. Rev. Ecol. Evol. Syst. 2003, 34, 239–272. [Google Scholar] [CrossRef]
  242. Clem, R.J.; Passarelli, A.L. Baculoviruses: Sophisticated pathogens of insects. PLoS Pathog. 2013, 9, e1003729. [Google Scholar] [CrossRef]
  243. Weseloh, R.M. People and the gypsy moth: A story of human interactions with an invasive species. Am. Entomol. 2003, 49, 180–190. [Google Scholar] [CrossRef] [Green Version]
  244. Doane, C.C. Ecology of pathogens of the gypsy moth. In Perspectives in Forest Entomology; Anderson, J.F., Kaya, H.K., Eds.; Academic Press: New York, NY, USA, 1976; pp. 285–293. [Google Scholar]
  245. Shapiro, M.; Bell, R.A.; Owens, C.D. In vivo mass production of gypsy moth nucleopolyhedrosis virus. In The Gypsy Moth; Research toward Integrated Pest Management; Doane, C.C., McManus, M.L., Eds.; USDA Technical Bulletin 1584; USDA: Washington, DC, USA, 1981; pp. 633–655. [Google Scholar]
  246. Lewis, F.B.; Yendol, W.G. Efficacy [of virus]. U.S. Dep. Agric. For. Serv. Tech. Bull. 1981, 1584, 503–512. [Google Scholar]
  247. Ruiu, L.; Mannu, R.; Olivieri, M.; Lentini, A. Gypsy Moth Management with LdMNPV Baculovirus in Cork Oak Forest. Forests 2021, 12, 495. [Google Scholar] [CrossRef]
  248. McManus, M.L.; Solter, L.F. Microsporidian pathogens in European gypsy moth populations. In Ecology, Survey and Management of Forest Insects; General Technical Report NE-311; McManus, M.L., Liebhold, A.M., Eds.; USDA Forest Service: Newton Square, PA, USA, 2003; pp. 44–51. [Google Scholar]
  249. Goertz, D.; Hoch, G. Horizontal transmission pathways of terrestrial microsporidia: A quantitative comparison of three pathogens infecting different organs in Lymantria dispar L. (Lep.: Lymantriidae) larvae. Biol. Control 2008, 44, 196–206. [Google Scholar] [CrossRef]
  250. Goertz, D.; Hoch, G. Vertical transmission and overwintering of microsporidia in the gypsy moth, Lymantria dispar. J. Invertebr. Pathol. 2008, 99, 43–48. [Google Scholar] [CrossRef]
  251. Hoch, G.; Zubrik, M.; Novotny, J.; Schopf, A. The natural enemy complex of the gypsy moth, Lymantria dispar (Lep., Lymantriidae) in different phases of its population dynamics in eastern Austria and Slovakia—A comparative study. J. Appl. Entomol. 2001, 125, 217–227. [Google Scholar] [CrossRef]
  252. Bathon, H. Biologische Bek€ Bekämpfung des Schwammspinners: Räuber und Parasitoide. In Schwammspinner-Kalamität im Forst; Wulf, A.B., Berendes, K.H., Eds.; Mitteilungen aus der Biologischen Bundesanstalt für Land- und Forstwirtschaft: Berlin, Germany, 1993; pp. 117–124. [Google Scholar]
  253. Bierl, B.A.; Beroza, M.; Collier, C.W. Potent sex attractant of the gypsy moth: Its isolation, identification and synthesis. Science 1970, 170, 87–89. [Google Scholar] [CrossRef]
  254. Beroza, M.; Knipling, E.F. Gypsy moth control with the sex attractant pheromone. Science 1972, 177, 19–27. [Google Scholar] [CrossRef] [PubMed]
  255. Brown, R.C.; Sheals, R.A. The present outlook on the gypsy moth problem. J. For. 1944, 42, 393–407. [Google Scholar]
  256. Mastro, V.C.; Richerson, J.V.; Cameron, E.A. An evaluation of gypsy moth pheromone-baited traps using behavioral observations as a measure of trap efficiency. Environ. Entomol. 1977, 6, 128–132. [Google Scholar] [CrossRef]
  257. Elkinton, J.S.; Childs, R.D. Efficiency of two gypsy moth (Lepidoptera: Lymantriidae) pheromone-baited traps. Environ. Entomol. 1983, 12, 1519–1525. [Google Scholar] [CrossRef]
  258. Thorpe, K.W.; Ridgway, R.L.; Leonhardt, B.A. Relationship between gypsy moth (Lepidoptera: Lymantriidae) pheromone trap catch and population density: Comparison of traps baited with 1 and 500 mg (þ)-disparlure lures. J. Econ. Entomol. 1993, 86, 86–92. [Google Scholar] [CrossRef]
  259. Richerson, J.V. Pheromone-mediated behavior of the gypsy moth. J. Chem. Ecol. 1977, 3, 291–301. [Google Scholar] [CrossRef]
  260. Liebhold, A.M.; Tobin, P.C. Population ecology of insect invasions and their management. Annu. Rev. Entomol. 2008, 53, 387–408. [Google Scholar] [CrossRef]
  261. Suckling, D.M.; Tobin, P.C.; McCullough, D.G.; Herms, D.A. Combining tactics to exploit Allee effects for eradication of alien insect populations. J. Econ. Entomol. 2012, 105, 1–13. [Google Scholar] [CrossRef]
  262. Epanchin-Niell, R.S.; Haight, R.G.; Berec, L.; Kean, J.M.; Liebhold, A.M. Optimal surveillance and eradication of invasive species in heterogeneous landscapes. Ecol. Lett. 2012, 15, 803–812. [Google Scholar] [CrossRef]
  263. Tobin, P.C.; Onufrieva, K.S.; Thorpe, K.W. The relationship between male moth density and female mating success in invading populations of Lymantria dispar. Entomol. Exp. Appl. 2013, 146, 103–111. [Google Scholar] [CrossRef]
  264. Miller, J.R.; Gut, L.J. Mating disruption for the 21st century: Matching technology with mechanism. Environ. Entomol. 2015, 44, 427–453. [Google Scholar] [CrossRef] [PubMed]
  265. Cardé, R.; Minks, A.K. Control of moths by mating disruption: Successes and constraints. Annu. Rev. Entomol. 1995, 40, 559–585. [Google Scholar] [CrossRef]
  266. Rice, R.E.; Kirsch, P. Mating Disruption of Oriental Fruit Moth in the United States. Behavior-Modifying Chemicals for Insect Management; Marcel Dekker: New York, NY, USA, 1990; pp. 193–211. [Google Scholar]
  267. Bengtsson, M.; Karg, G.; Kirsch, P.A.; Lofqvist, J.; Sauer, A.; Witzgall, P. Mating Disruption of Pea Moth CydiaNigricana F (Lepidoptera, Tortricidae) by a Repellent Blend of Sex-Pheromone and Attraction Inhibitors. J. Chem. Ecol. 1994, 20, 871–887. [Google Scholar] [CrossRef] [PubMed]
  268. Witzgall, P.; Backman, A.C.; Svensson, M.; Koch, U.; Rama, F.; ElSayed, A.; Brauchli, J.; Arn, H.; Bengtsson, M.; Lofqvist, J. Behavioral observations of codling moth, Cydia pomonella, in orchards permeated with synthetic pheromone. Biocontrol 1999, 44, 211–237. [Google Scholar] [CrossRef]
  269. Thorpe, K.; Reardon, R.; Tcheslavskaia, K.; Leonard, D.; Mastro, V. A Review of the Use of Mating Disruption to Manage Gypsy Moth, Lymantria dispar (L.). Available online: http://www.fs.fed.us/foresthealth/technology/pdfs/GMComplete.pdf (accessed on 29 June 2022).
  270. Walton, V.M.; Daane, K.M.; Bentley, W.J.; Millar, J.G.; Larsen, T.E.; Malakar-Kuenen, R. Pheromone-based mating disruption of Planococcus ficus (Hemiptera: Pseudococcidae) in California vineyards. J. Econ. Entomol. 2006, 99, 1280–1290. [Google Scholar] [CrossRef]
  271. Stelinski, L.L.; Gut, L.J.; Miller, J.R. An attempt to increase efficacy of moth mating Disruption by Co-releasing pheromones with kairomones and to understand possible underlying mechanisms of this technique. Environ. Entomol. 2013, 42, 158–166. [Google Scholar] [CrossRef] [Green Version]
  272. Trematerra, P.; Colacci, M.; Athanassiou, C.G.; Kavallieratos, N.G.; Rumbos, C.; Boukouvala, M.C.; Nikolaidou, A.J.; Kontodimas, D.C.; Benavent-Fernández, E.; Gálvez-Settier, S. Evaluation of Mating disruption for the control of Thaumetopoea pityocampa (Lepidoptera: Thaumetopoeidae) in suburban recreational areas in Italy and Greece. J. Econ. Entomol. 2019, 112, 2229–2235. [Google Scholar] [CrossRef]
  273. Gordon, D.; Zahavi, T.; Anshelevich, L.; Harel, M.; Ovadia, S.; Dunkelblum, E.; Harari, A.R. Mating disruption of Lobesia botrana (Lepidoptera: Tortricidae): Effect of pheromone formulations and concentrations. J. Econ. Entomol. 2005, 98, 135–142. [Google Scholar] [CrossRef]
  274. Stelinski, L.L.; Miller, J.R.; Ledebuhr, R.; Siegert, P.; Gut, L.J. Season-long mating disruption of Grapholita molesta (Lepidoptera: Tortricidae) by one machine application of pheromone in wax drops (SPLAT-OFM). J. Pest Sci. 2007, 80, 109–117. [Google Scholar] [CrossRef]
  275. Hoshi, H.; Takabe, M.; Nakamuta, K. Mating disruption of a carpenter moth, Cossus insularis (Lepidoptera: Cossidae) in apple orchards with synthetic sex pheromone, and registration of the pheromone as an agrochemical. J. Chem. Ecol. 2016, 42, 606–611. [Google Scholar] [CrossRef]
  276. Mori, B.A.; Evenden, M.L. When mating disruption does not disrupt mating: Fitness consequences of delayed mating in moths. Entomol. Exp. Appl. 2013, 146, 50–65. [Google Scholar] [CrossRef]
  277. Tobin, P.C.; Bolyard, J.L.; Onufrieva, K.S.; Hickman, A.D. The effect of male and female age on Lymantria dispar (Lepidoptera: Lymantriidae) fecundity. J. Econ. Entomol. 2014, 107, 1076–1083. [Google Scholar] [CrossRef] [PubMed]
  278. Hide, R.; Suckling, D. Decision analysis of insecticide resistance in light-brown apple moth. N. Z. J. Exp. Agric. 1988, 16, 219–224. [Google Scholar] [CrossRef]
  279. Suckling, D.; Shaw, P.; Khoo, J.; Cruickshank, V. Resistance management of lightbrown apple moth, Epiphyas postvittana (Lepidoptera: Tortricidae) by mating disruption. N. Z. J. Crop Hortic. Sci. 1990, 18, 89–98. [Google Scholar] [CrossRef]
  280. Caprio, M.A.; Suckling, D.M. Mating Disruption Reduces the Risk of Resistance Development to Transgenic Apple Orchards: Simulations of the Lightbrown Apple Moth: New Zealand; Plant Protection Society: Rotorua, New Zeland, 1995; pp. 52–58. [Google Scholar]
  281. Schwalbe, C.P.; Mastro, V.C. Gypsy moth mating disruption: Dosage effects. J. Chem. Ecol. 1988, 14, 581–588. [Google Scholar] [CrossRef]
  282. Leonhardt, B.A.; Mastro, V.C.; Leonard, D.S.; McLane, W.; Reardon, R.C.; Thorpe, K.W. Control of low-density gypsy moth (Lepidoptera: Lymantriidae) populations by mating disruption with pheromone. J. Chem. Ecol. 1996, 22, 1255–1272. [Google Scholar] [CrossRef]
  283. Thorpe, K.W.; Mastro, V.C.; Leonard, D.S.; Leonhardt, B.A.; McLane, W.; Reardon, R.C.; Talley, S.E. Comparative efficacy of two controlled-release gypsy moth mating disruption formulations. Entomol. Exp. Appl. 1999, 90, 267–277. [Google Scholar] [CrossRef]
  284. Onufrieva, K.S.; Thorpe, K.W.; Hickman, A.D.; Leonard, D.S.; Mastro, V.C.; Roberts, E.A. Gypsy moth mating disruption in open landscapes. Agric. For. Entomol. 2008, 10, 175–179. [Google Scholar] [CrossRef]
  285. Collins, C.W.; Hood, C.E. Gypsy Moth Tree Banding Material: How to Make, Use, and Apply It; Bulletin 899; United States Department of Agriculture: Washington, DC, USA, 1920. [Google Scholar]
  286. McManus, M.L.; Houston, D.R.; Wallner, W.E. The Homeowner and the Gypsy Moths: Guidelines for Control; Home and Garden Bulletin No. 227; USDA: Washington, DC, USA, 1980; p. 34. [Google Scholar]
  287. McManus, M.L.; Smith, H.R. Effectiveness of Artificial Bark Flaps in Mediating Migration of Late-Instar Gypsy Moth Larvae; Forest Service Res. NE-316; U.S. Department of Agriculture: Washington, DC, USA, 1984. [Google Scholar]
  288. Liebhold, A.M.; Elkinton, J.S.; Wallner, W.E. Effect of burlap bands on between-tree movement of late-instar gypsy moth, Lymantria dispar (Lepidoptera:Lymantriidae). Environ. Entomol. 1986, 15, 373–379. [Google Scholar] [CrossRef]
  289. Blumenthal, E.M.; Hoover, C.R. Gypsy moth (Lepidoptera: Lymantriidae) population control using mechanical barriers and contact insecticides applied to tree stems. J. Econ. Entomol. 1986, 79, 1394–1396. [Google Scholar] [CrossRef]
  290. Thorpe, K.W.; Webb, R.E.; Ridgway, R.L.; Venables, L.; Tatman, K.M. Sticky barrier bands affect density of Gypsy moth (Lepidoptera:Lymantriidae) and damage in oak canopies. J. Econ. Entomol. 1993, 86, 1479–1501. [Google Scholar] [CrossRef]
  291. Bell, J.L.; Whitmore, R.C. Bird populations and habitat in Bacillus thuringiensis and Dimilin-treated and untreated areas of hardwood forest. Am. Midl. Nat. 1997, 137, 239–250. [Google Scholar] [CrossRef]
  292. Conis, E. Polio, DDT, and disease risk in the United States after World War II. Environ. Hist. 2017, 22, 696–721. [Google Scholar] [CrossRef]
  293. Allstadt, A.J.; Haynes, K.J.; Liebhold, A.M.; Johnson, D.M. Long-term shifts in the cyclicity of outbreaks of a forest-defoliating insect. Oecologia 2013, 172, 141–151. [Google Scholar] [CrossRef]
  294. Schönfeld, F. Dimilin im Eichenwald—Insektizideinsatz mit Nebenwirkungen. LWF Aktuell 2009, 70, 58–60. [Google Scholar]
  295. Durkin, P.R. Control/Eradication Agents for the Gypsy Moth—Human Health and Ecological Risk Assessment for Bacillus thuringiensis var. Kurstaki (B.t.k.); SERA Technical Reports, 03-43-05-02d, (4-1–4-25); U.S. Department of Agriculture, Forest Service, Forest Health: Arlington, WA, USA, 2004. [Google Scholar]
  296. Protection European Food Safety Authority. Conclusion on the peer review of the pesticide risk assessment of confirmatory data submitted for the active substance diflubenzuron. EFSA J. 2012, 10, 2870. [Google Scholar] [CrossRef]
  297. Lemme, H.; Lobinger, G.; Müller-Kroehling, S. Schwammspinner—Massenvermehrung in Franken. LWF Aktuell 2019, 121, 37–43. [Google Scholar]
  298. Sial, A.A.; Brunner, J.F. Toxicity and residual efficacy of Chlorantraniliprole, Spinetoram, and Emamectin benzoate to Obliquebanded Leafroller (Lepidoptera: Tortricidae). J. Econ. Entomol. 2010, 103, 1277–1285. [Google Scholar] [CrossRef]
  299. Ishtiaq, M.; Razaq, M.; Saleem, M.A.; Anjumm, F.; Noor ul An, M.; Raza, A.M.; Wright, D.J. Stability, cross-resistance and fitness costs of resistance to emamectin benzoate in a re-selected field population of the beet armyworm, Spodoptera exigua (Lepidoptera: Noctuidae). Crop Prot. 2014, 65, 227–231. [Google Scholar] [CrossRef]
  300. Xu, Z.; Bai, J.; Li, L.u.; Liang, L.; Ma, X.; Ma, L. Sublethal concentration of emamectin benzoate inhibits the growth of gypsy moth by inducing digestive dysfunction and nutrient metabolism disorder. Pest Manag. Sci. 2021, 77, 4073–4083. [Google Scholar] [CrossRef]
  301. Oberemok, V.V.; Laikova, K.V.; Zaitsev, A.S.; Nyadar, P.M.; Gninenko, Y.I.; Gushchin, V.A.; Makarov, V.V.; Agranovsky, A.A. Topical treatment of LdMNPV-infected gypsy moth caterpillars with 18 nucleotides long antisense fragment from LdMNPV IAP-3 gene triggers higher levels of apoptosis in the infected cells and mortality of the pest. J. Plant Prot. Res. 2017, 57, 18–24. [Google Scholar] [CrossRef]
  302. Oberemok, V.V.; Laikova, K.V.; Repetskaya, A.I.; Kenyo, I.M.; Gorlov, M.V.; Kasich, I.N.; Krasnodubets, A.M.; Gal’chinsky, N.V.; Fomochkina, I.I.; Zaitsev, A.S.; et al. A half-century history of applications of antisense oligonucleotides in medicine, agriculture and forestry: We should continue the journey. Molecules 2018, 23, 1302. [Google Scholar] [CrossRef] [PubMed]
  303. Wang, Y.; Zhang, H.; Li, H.; Miao, X. Second-generation sequencing supplies an effective way to screen RNAi targets in large scale for potential application in pest insect control. PLoS ONE 2011, 6, e18644. [Google Scholar] [CrossRef] [PubMed]
  304. Gu, L.; Knipple, D.C. Recent advances in RNA interference research in insects: Implications for future insect pest management strategies. Crop Prot. 2013, 45, 36–40. [Google Scholar] [CrossRef]
  305. Oberemok, V.V.; Laikova, K.V.; Useinov, R.Z.; Gal’chinsky, N.V.; Novikov, I.A.; Yurchenko, K.A.; Volkov, M.E.; Gorlov, M.V.; Brailko, V.A.; Plugatar, Y.V. Insecticidal activity of three 10–12 nucleotides long antisense sequences from 5.8S ribosomal RNA gene of gypsy moth Lymantria dispar L. against its larvae. J. Plant Prot. Res. 2019, 59, 561–564. [Google Scholar]
  306. Oberemok, V.V.; Laikova, K.V.; Gal’chinsky, N.V.; Useinov, R.Z.; Novikov, I.A.; Temirova, Z.Z.; Shumskykh, M.N.; Krasnodubets, A.M.; Repetskaya, A.I.; Dyadichev, V.V.; et al. DNA insecticide developed from the Lymantria dispar 5.8S ribosomal RNA gene provides a novel biotechnology for plant protection. Sci. Rep. 2019, 9, 6197. [Google Scholar] [CrossRef]
  307. Oberemok, V.V.; Laikova, K.V.; Zaitsev, A.S.; Shumskykh, M.N.; Kasich, I.N.; Gal’chinsky, N.V.; Bekirova, V.V.; Makarov, V.V.; Agranovsky, A.A.; Gushchin, V.A.; et al. Molecular alliance of Lymantria dispar multiple nucleopolyhedrovirus and a short unmodified antisense oligonucleotide of its anti-apoptotic IAP-3 gene: A novel approach for gypsy moth control. Int. J. Mol. Sci. 2017, 18, 2446. [Google Scholar] [CrossRef]
  308. Stenersen, J. Chemical Pesticides Mode of Action and Toxicology, 1st ed.; CRC Press: Boca Raton, FL, USA, 2004. [Google Scholar]
  309. Devine, G.J.; Furlong, M.J. Insecticide use: Contexts and ecological consequences. Agric. Hum. Values 2007, 24, 281–306. [Google Scholar] [CrossRef]
  310. Guedes, R.N.C.; Walse, S.S.; Throne, J.E. Sublethal exposure, insecticide resistance, and community stress. Curr. Opin. Insect Sci. 2017, 21, 47–53. [Google Scholar] [CrossRef] [Green Version]
  311. Brevik, K.; Schoville, S.D.; Mota-Sanchez, D.; Chen, Y.H. Pesticide durability and the evolution of resistance: A novel application of survival analysis. Pest Manag. Sci. 2018, 74, 1953–1963. [Google Scholar] [CrossRef]
  312. Umina, P.A.; McDonald, G.; Maino, J.; Edwards, O.; Hoffmann, A.A. Escalating insecticide resistance in Australian grain pests: Contributing factors, industry trends and management opportunities. Pest Manag. Sci. 2019, 75, 1494–1506. [Google Scholar] [CrossRef] [PubMed]
  313. Dar, M.A.; Kaushik, G.; Chiu, J.F.V. Pollution status and biodegradation of organophosphate pesticides in the environment. In Abatement of Environmental Pollutants; Singh, P., Kumar, A., Borthakur, A., Eds.; Elsevier: Amsterdam, The Netherlands, 2020; pp. 25–66. [Google Scholar]
  314. Senthil-Nathan, S. A review of bio pesticides and their mode of action against insect pests. In Environmental Sustainability—Role of Green Technologies; Thangavel, P., Sridevi, G., Eds.; Springer: New Delhi, India, 2015; pp. 49–63. [Google Scholar]
  315. Kumar, V. A review on efficacy of biopesticides to control the agricultural insect’s pest. Int. J. Agric. Sci. Res. 2015, 4, 168–179. [Google Scholar]
  316. Anwer, M.A. Biopesticides and Bioagents: Novel Tools for Pest Management, 1st ed.; CRC Press: Boca Raton, FL, USA, 2017. [Google Scholar]
  317. Isman, M.B. Commercial development of plant essential oils and their constituents as active ingredients in bioinsecticides. Phytochem. Rev. 2020, 19, 235–241. [Google Scholar] [CrossRef]
  318. Stanković, S.; Kostić, M.; Kostić, I.; Krnjajić, S. Practical approaches to pest control: The use of natural compounds. In Pests, Weeds and Diseases in Agricultural Crop and Animal Husbandry Production; Kontogiannatos, D., Ed.; IntechOpen: London, UK, 2020; pp. 43–60. [Google Scholar]
  319. Shahzad, K.; Manzoor, F. Nanoformulations and their mode of action in insects: A review of biological interactions. Drug Chem. Toxicol. 2021, 44, 1–11. [Google Scholar] [CrossRef]
  320. Helson, B. Naturally derived insecticides: Prospects for forestry use. For. Chron. 1992, 68, 349–354. [Google Scholar] [CrossRef]
  321. Kostić, I.; Lazarević, J.; Šešlija Jovanović, D.; Kostić, M.; Marković, T.; Milanović, S. Potential of Essential Oils from Anise, Dill and Fennel Seeds for the Gypsy Moth Control. Plants 2021, 10, 2194. [Google Scholar] [CrossRef]
  322. Carson, F.; Hammer, K.A. Chemistry and bioactivity of essential oils. In Lipids and Essential Oils as Antimicrobial Agents; Thormar, H., Ed.; John Wiley & Sons: London, UK, 2011; Volume 25, pp. 203–238. [Google Scholar]
  323. Koul, O. Phytochemicals and insect control: An antifeedant approach. Crit. Rev. Plant Sci. 2008, 27, 1–24. [Google Scholar] [CrossRef]
  324. Trumble, J.T. Caveat emptor: Safety considerations for natural products used in arthropod control. Am. Entomol. 2002, 48, 7–13. [Google Scholar] [CrossRef]
  325. Trongtokit, Y.; Rongsriyam, Y.; Komalamisra, N.; Apiwathnasorn, C. Comparative repellency of 38 essential oils against mosquito bites. Phytother. Res. 2005, 19, 303–309. [Google Scholar] [CrossRef]
  326. Katz, M.; Miller, H.; Hebert, A. Insect repellents: Historical perspectives and new developments. J. Am. Acad. Dermatol. 2008, 58, 865–871. [Google Scholar] [CrossRef]
  327. Regnault-Roger, C.; Vincent, C.; Arnason, J.T. Essential oils in insect control: Low-risk products in a high-stakes world. Annu. Rev. Entomol. 2012, 57, 405–424. [Google Scholar] [CrossRef]
  328. Pavela, R.; Benelli, G. Essential oils as ecofriendly biopesticides? Challenges and constraints. Trends. Plant Sci. 2016, 21, 1000–1007. [Google Scholar] [CrossRef]
  329. Moretti, L.; Sanna-Passino, G.; Demontis, S.; Bazzoni, E. Essential oil formulations useful as a new tool for insect pest control. AAPS Pharm. Sci. Tech. 2002, 3, e13. [Google Scholar] [CrossRef] [PubMed]
  330. Kostić, I.; Petrović, O.; Milanović, S.; Popović, Z.; Stanković, S.; Todorović, G.; Kostić, M. Biological activity of essential oils of Athamanta haynaldii and Myristica fragrans to gypsy moth larvae. Ind. Crop Prod. 2013, 41, 17–20. [Google Scholar] [CrossRef]
  331. Devrnja, N.; Kostić, I.; Lazarević, J.; Savić, J.; Ćalić, D. Evaluation of tansy essential oil as potential ‘green’ alternative for gypsy moth control. Environ. Sci. Pollut. Res. 2020, 27, 11958–11967. [Google Scholar] [CrossRef] [PubMed]
  332. Devrnja, N.; Anđelković, B.; Aranđelović, S.; Radulović, S.; Soković, M.; Krstić-Milošević, D.; Ristić, M.; Ćalić, D. Comparative studies on the antimicrobial and cytotoxic activities of Tanacetum vulgare L. essential oil and methanol extracts. S. Afr. J. Bot. 2017, 111, 212–221. [Google Scholar] [CrossRef]
  333. Berry, E.; Moldenke, F.; Miller, C.; Wernz, G. Toxicity of diflubenzuron in larvae of gypsy moth (Lepidoptera: Lymantriidae): Effects of host plant. J. Econ. Entomol. 1993, 86, 809–814. [Google Scholar] [CrossRef]
  334. Traupman, J.C. The Bantam New College Latin and English Dictionary, 2nd ed.; Bantam Books: New York, NY, USA, 1995. [Google Scholar]
  335. Hellier, F.F.; Warin, R.P. Caterpillar dermatitis. Br. Med. J. 1967, 2, 346–348. [Google Scholar] [CrossRef]
  336. Haddad, V., Jr.; Lastória, J.C. Envenomation by caterpillars (erucism): Proposal for simple pain relief treatment. J. Venom Anim. Toxins Incl. Trop. Dis. 2014, 20, 21. [Google Scholar] [CrossRef]
  337. Goldman, L.; Sawyer, F.; Levine, A.; Goldman, J.; Goldman, S.; Spinanger, J. Investigative studies of skin irritations from caterpillars. J. Investig. Dermatol. 1960, 34, 67–79. [Google Scholar] [CrossRef] [Green Version]
  338. Haddad, V., Jr.; Cardoso, J.L.C. Erucismo e lepidopterismo. In Animais Peçonhentos No Brasil: Biologia, Clínica e Terapêutica Dos Acidentes; Cardoso, J.L.C., Franca, F.O.S., Wen, F.H., Malaque, C.M.S., Haddad, V., Jr., Eds.; Sarvier: São Paulo, Brazil, 2003; pp. 236–239. [Google Scholar]
  339. Cardoso, A.E.C.; Haddad, V., Jr. Acidentes por lepidópteros (larvas e adultos de mariposas): Estudo dos aspectos epidemiológicos, clínicos e terapêuticos. An. Bras. Dermatol. 2005, 80, 571–578. [Google Scholar] [CrossRef]
  340. Haddad, V., Jr.; Cardoso, J.L.; Lupi, O.; Tyring, S.K. Tropical dermatology: Venomous arthropods and human skin: Part I: Insecta. J. Am. Acad. Dermatol. 2012, 67, 331. [Google Scholar] [CrossRef] [PubMed]
  341. Stipetic, M.E.; Rosen, P.B.; Borys, D.J. A retrospective analysis of 96 “Asp” (Megalopyge opercularis) envenomations in central Texas during 1996. J. Toxicol. Clin. Toxicol. 1999, 37, 457–462. [Google Scholar] [CrossRef] [PubMed]
  342. Battisti, A.; Holm, G.; Fagrell, B.; Larsson, S. Urticating Hairs in Arthropods: Their Nature and Medical Significance. Annu. Rev. Entomol. 2011, 56, 203–210. [Google Scholar] [CrossRef]
  343. Shama, S.K.; Etkind, P.H.; Odell, T.M.; Canada, A.T.; Finn, A.M.; Soter, N.A. Gypsy-moth-caterpillar-dermatitis. N. Engl. J. Med. 1982, 306, 1300–1301. [Google Scholar] [CrossRef]
  344. Beaucher, W.N.; Farnham, J.E. Gypsymoth-caterpillar dermatitis. N. Engl. J. Med. 1982, 21, 1301–1302. [Google Scholar] [CrossRef]
  345. De Jong, M.C.; Bleumink, E. Investigative studies of the dermatitis caused by the larva of the brown-tail moth, Euproctis chrysorrhoea L. (Lepidoptera, Lymantriidae). Arch. Dermatol. Res. 1977, 259, 247–262. [Google Scholar] [CrossRef]
  346. Croitoru, D.O.; Brooks, S.G.; Pon, K. Dermatitis after exposure to Lymantria dispar dispar. Can. Med. Assoc. J. 2022, 194, E500. [Google Scholar] [CrossRef]
  347. Deml, R. Pyrrolidinyl and pyridyl alkaloids in Lymantria dispar. Z. Naturforsch. C Biosci. 2003, 58, 860–866. [Google Scholar] [CrossRef]
  348. Villas-Boas, I.M.; Bonfá, G.; Tambourgi, D.V. Venomous caterpillars: From inoculation apparatus to venom composition and envenomation. Toxicon 2018, 153, 39–52. [Google Scholar] [CrossRef]
  349. Aldrich, J.R.; Schaefer, P.W.; Oliver, J.E.; Puapoomchareon, P.; Lee, C.J.; Vander Meer, R.K. Biochemistry of the exocrine secretion from gypsy moth caterpillars (Lepidoptera: Lymantriidae). Ann. Entomol. Soc. Am. 1997, 90, 75–82. [Google Scholar] [CrossRef]
  350. Teutschlaender, O. Ueber die durch Rauperhaare Verursachten Erkrankungen. Arch. Augenheilkd. 1908, 61, 117–118. [Google Scholar]
  351. Perlman, F.; Press, E.; Googins, J.A.; Malley, A.; Poarea, H. Tussockosis: Reactions to Douglas fir tussock moth. Ann. Allergy 1976, 36, 302–307. [Google Scholar] [PubMed]
  352. Anderson, J.F.; Furniss, W.E. Epidemic of urticaria associated with first-instar larvae of the gypsy moth (Lepidoptera: Lymantriidae). J. Med. Entomol. 1983, 20, 146–150. [Google Scholar] [CrossRef]
  353. Tuthill, R.W.; Canada, A.T.; Wilcock, K.; Etkind, P.H.; O’Dell, T.M.; Sharma, S.K. An epidemiologic study of gypsy moth rash. Am. J. Public Health 1984, 74, 799–803. [Google Scholar] [CrossRef] [PubMed]
  354. Wirtz, R.A. Occupational allergies to arthropods—Documentation and prevention. Bull. Entomol. Soc. Am. 1980, 26, 356–360. [Google Scholar] [CrossRef]
  355. Etkind, P.H.; Odell, T.M.; Canada, A.T.; Shama, S.K.; Finn, A.M.; Tuthill, R.W. The gypsy moth caterpillar: A significant new occupational and public health problem. J. Occup. Med. 1982, 24, 659–662. [Google Scholar] [CrossRef] [PubMed]
  356. Steen, C.J.; Carbonaro, P.A.; Schwartz, R.A. Arthropods in dermatology. J. Am. Acad. Dermatol. 2004, 50, 819–842. [Google Scholar] [CrossRef]
  357. Haq, M.; O’Toole, A.; Beecker, J.; Gooderham, M.J. Return of Lymantria dispar dispar (gypsy moth): A case report. SAGE Open Med. Case Rep. 2021, 9, 2050313X211057926. [Google Scholar] [CrossRef]
  358. Gooderham, M.; Haq, M.; Beecker, J.; O’Toole, A. Lymantria dispar dispar (Gypsy) moth dermatitis. J. Cutan. Med. Surg. 2021, 25, 555–556. [Google Scholar] [CrossRef]
  359. Kikuchi, T.; Kobayashi, K.; Sakata, K.; Akasaka, T. Gypsy moth-induced dermatitis: A hospital review and community survey. Eur. J. Dermatol. 2012, 22, 384–390. [Google Scholar] [CrossRef] [PubMed]
  360. Hossler, E.W. Caterpillars and moths. Part I: Dermatologic manifestations of encounters with Lepidoptera. J. Am. Acad. Dermatol. 2010, 62, 1–10. [Google Scholar] [CrossRef] [PubMed]
  361. Lin, W.; Yu, Y.; Zhou, P.; Zhang, J.; Dou, L.; Hao, Q.; Chen, H.; Zhu, S. Identification and Knockdown of the Olfactory Receptor (OrCo) in Gypsy Moth, Lymantria dispar. Int. J. Biol. Sci. 2015, 11, 772–780. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  362. European Parliament. Directive 2009/128/CE of the European Parliament and of the Council of 21 October 2009 Establishing a Framework for Community Action to Achieve the Sustainable Use of Pesticides. Available online: https://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2009:309:0071:0086:en:PDF (accessed on 6 September 2022).
Figure 1. (a) Severe defoliation of oak by Lymantria dispar. (b) Egg clusters of L. dispar. (c) Late instar larva of L. dispar. (d) Pupa of L. dispar. (e) Newly emerged adult male of L. dispar. (f) Female of L. dispar laying eggs on a wall.
Figure 1. (a) Severe defoliation of oak by Lymantria dispar. (b) Egg clusters of L. dispar. (c) Late instar larva of L. dispar. (d) Pupa of L. dispar. (e) Newly emerged adult male of L. dispar. (f) Female of L. dispar laying eggs on a wall.
Insects 13 00854 g001aInsects 13 00854 g001b
Table 1. Susceptible, preferred, and resistant tree species to Lymantria dispar larvae.
Table 1. Susceptible, preferred, and resistant tree species to Lymantria dispar larvae.
Common NameScientific NameOrderFamilyCategorizationReference
European crab appleMalus sylvestris (L.) Mill.RosalesRosaceaeSusceptible[17]
Bigtooth aspenPopulus grandidentata MichauxMapighialesSalicaceaeSusceptible[17]
Quaking aspenP. tremuloides Michx.MapighialesSalicaceaeSusceptible[17]
BoxelderAcer negundo L.SapindalesSapindaceaeSusceptible[17]
American mountain ashSorbus americana MarshallRosalesRosaceaeSusceptible[17]
SweetgumLiquidambar styraciflua L.SaxifragalesAltingiaceaeSusceptible[17]
BasswoodTilia spp.MalvalesMalvaceaeSusceptible[17]
BirchBetula spp.FagalesBetulaceaeSusceptible[17]
LarchLarix spp.PinalesPinaceaeSusceptible[17]
OakQuercus spp.FagalesFagaceaeSusceptible[17]
WillowSalix spp.MalpighialesSalicaceaeSusceptible[17]
AlderAlnus spp.FagalesBetulaceaePreferred[10]
HawthornCrataegus spp.RosalesRosaceaePreferred[10]
HazelnutCorylus spp.FagalesBetulaceaePreferred[10]
HornbeamCarpinus sp.FagalesBetulaceaePreferred[10]
ServiceberryAmelanchier spp.RosalesRosaceaePreferred[10]
SumacRhus spp.SapindalesAnacardiaceaePreferred[10]
HemlockTsuga canadensis (L.) CarrièrePinalesPinaceaeResistant[10,17]
Yellow birchBetula alleghaniensis Britt.FagalesBetulaceaeResistant[10,17]
Eastern white pinePinus strobus L.PinalesPinaceaeResistant[10,17]
Table 2. Predators and parasitoids of Lymantria dispar larvae.
Table 2. Predators and parasitoids of Lymantria dispar larvae.
Predators
Species NameOrderFamilyReference
Peromyscus leucopus (Rafinesque, 1818)RodentiaCricetidae[194]
Apodemus sylvaticus (Linnaeus, 1758)RodentiaMuridae[59,169]
Crocidura russula (Hermann, 1780)EulipotyphlaSoricidae[59,169]
Parus major Linnaeus, 1758PasseriformesParidae[59,169]
Garrulus glandarius (Linnaeus, 1758)PasseriformesCorvidae[59,169]
Dendrocopos kizuki (Temminck, 1836)PasseriformesPicidae[59,169]
Sitta eiuropaea Linnaeus, 1758PasseriformesSittidae[59,169]
Calosoma sycophanta L.ColeopteraCarabidae[56,59,169,195,196,197,198,199,200,201,202,203]
Parasitoids
Acropimpla didyma (Gravenhorst)HymenopteraIchneumonidae[44]
Aleiodes pallidator ThunbergHymenopteraBraconidae[44]
Anastatus bifasciatus (Geoffroy)HymenopteraEupelmidae[44]
Anastatus catalonicus Bolivar & PieltainHymenopteraEupelmidae[44]
Anastatus japonicus AshmeadHymenopteraEupelmidae[44]
Apanteles impurus (Nees)HymenopteraBraconidae[44]
Apanteles lacteicolor ViereckHymenopteraBraconidae[44]
Apanteles xanthostigma (Haliday)HymenopteraBraconidae[44]
Apechthis capulifera (Kriechbaumer)HymenopteraIchneumonidae[44]
Apechthis compunctor (L.)HymenopteraIchneumonidae[44]
Apechthis quadridentata (Thomson)HymenopteraIchneumonidae[44]
Apechthis rufata (Gmelin)HymenopteraIchneumonidae[44]
Aphantorhaphopsis samarensis (Villeneuve)DipteraTachinidae[44]
Banchus falcatorius (Fabricius)HymenopteraIchneumonida[44]
Barylypa pallida (Gravenhorst)HymenopteraIchneumonida[44]
Baryscapus oophagus (Otten)HymenopteraEulophidae[44]
Blepharipa pratensis (Meigen)DipteraTachinidae[44]
Blepharipa schineri (Mesnil)DipteraTachinidae[44]
Blondelia nigripes (Fallén)DipteraTachinidae[44]
Blondelia piniariae (Hartig)DipteraTachinidae[44]
Bothriothorax altensteinii RatzeburgHymenopteraEncyrtidae[44]
Bothriothorax paradoxus DalmanHymenopteraEncyrtidae[44]
Brachymeria inermis (Fonscolombe)HymenopteraChalcididae[44]
Brachymeria minuta (L.)HymenopteraChalcididae[44]
Brachymeria secundaria (Ruschka)HymenopteraChalcididae[44]
Brachymeria tibialis WalkerHymenopteraChalcididae[44]
Campoplex difformis (Gmelin)HymenopteraIchneumonidae[44]
Carcelia gnava (Meigen)DipteraTachinidae[44]
Casinaria tenuiventris (Gravenhorst)HymenopteraIchneumonidae[44]
Chouioia cunea YangHymenopteraEulophidae[44]
Cirrospilus pictus NeesHymenopteraEulophidae[44]
Compsilura concinnata (Meigen)DipteraTachinidae[44]
Cotesia gastropachae (Bouché)HymenopteraBraconidae[44]
Cotesia glomerata (L.)HymenopteraBraconidae[44]
Cotesia melanoscela (Ratzeburg)HymenopteraBraconidae[44]
Cotesia melitaearum (Wilkinson)HymenopteraBraconidae[44]
Cotesia neustriae (Tobias)HymenopteraBraconidae[44]
Cotesia ocneriae (Ivanov)HymenopteraBraconidae[44]
Cotesia praepotens (Haliday)HymenopteraBraconidae[44]
Cotesia rubripes (Haliday)HymenopteraBraconidae[44]
Cotesia spuria (Wesmael)HymenopteraBraconidae[44]
Deuterixys carbonaria (Wesmael)HymenopteraBraconidae[44]
Doryctes leucogaster (Nees)HymenopteraBraconidae[44]
Drino gilva (Hartig)DipteraTachinidae[44]
Drino inconspicua (Meigen)DipteraTachinidae[44]
Dusona blanda (Förster)HymenopteraIchneumonidae[44]
Elachertus charondas WalkerHymenopteraEulophidae[44]
Elasmus nudus NeesHymenopteraEulophidae[44]
Euceros serricornis (Haliday)HymenopteraIchneumonidae[44]
Euceros superbus KriechbaumerHymenopteraIchneumonidae[44]
Eulophus cyanescens BoučekHymenopteraEulophidae[44]
Eulophus larvarum L.HymenopteraEulophidae[44]
Eulophus slovacus BoučekHymenopteraEulophidae[44]
Eupelmus annulatus NeesHymenopteraEulophidae[44]
Eupelmus urozonus DalmanHymenopteraEulophidae[44]
Euplectrus liparidis FerrièreHymenopteraEulophidae[44]
Eurytoma appendigaster SwederusHymenopteraEurytomidae[44]
Eurytoma goidanichi BoučekHymenopteraEurytomidae[44]
Eurytoma verticillata (Fabricius)HymenopteraEurytomidae[44]
Exeristes roborator (Fabricius)HymenopteraIchneumonidae[44]
Exorista amoena (Mesnil)DipteraTachinidae[44]
Exorista larvarum (L.)DipteraTachinidae[44]
Exorista segregata (Rondani)DipteraTachinidae[44]
Gelis agilis (Fabricius)HymenopteraIchneumonidae[44]
Gelis areator (Panzer)HymenopteraIchneumonidae[44]
Glyptapanteles porthetriae (Muesebeck)HymenopteraBraconidae[44]
Glyptapanteles vitripennis (Curtis)HymenopteraBraconidae[44]
Gregopimpla inquisitor (Scopoli)HymenopteraIchneumonidae[44]
Gryon howardi (Mokrzecki and Oglobin)HymenopteraScelionidae[44]
Gryon hungaricum (Szabó)HymenopteraScelionidae[44]
Gryon lymantriae (Masner)HymenopteraScelionidae[44]
Hemiteles pulchellus GravenhorstHymenopteraIchneumonidae[44]
Hyposoter tricoloripes (Viereck)HymenopteraIchneumonidae[44]
Ichneumon sarcitorius L.HymenopteraIchneumonidae[44]
Iseropus stercorator (Fabricius)HymenopteraIchneumonidae[44]
Itoplectis alternans (Gravenhorst)HymenopteraIchneumonidae[44]
Itoplectis enslini (Ulbricht)HymenopteraIchneumonidae[44]
Itoplectis kolthoffi (Aurivillius)HymenopteraIchneumonidae[44]
Itoplectis viduata (Gravenhorst)HymenopteraIchneumonidae[44]
Lymantrichneumon disparis (Poda)HymenopteraIchneumonidae[44]
Lysibia nana (Gravenhorst)HymenopteraIchneumonidae[44]
Melittobia acasta WalkerHymenopteraEulophidae[44]
Mesochorus confusus HolmgrenHymenopteraIchneumonidae[44]
Meteorus pendulus (Müller)HymenopteraBraconidae[44]
Meteorus pulchricornis (Wesmael)HymenopteraBraconidae[44]
Meteorus versicolor (Wesmael)HymenopteraBraconidae[44]
*Monodontomerus aereus WalkerHymenopteraTorymidae[44]
Ooencyrtus kuvanae (Howard)HymenopteraEncyrtidae[44]
Ooencyrtus masii (Mercet)HymenopteraEncyrtidae[44]
Parasarcophaga uliginosa (Kramer)DipteraSarcophagidae[44]
Parasetigana silvestris (Robineau-Desvoidy)DipteraTachinidae[44]
Pediobius cassidae ErdösHymenopteraEulophidae[44]
Pediobius crassicornis (Thomson)HymenopteraEulophidae[44]
Pediobius foliorum (Geoffroy)HymenopteraEulophidae[44]
Pediobius pyrgo (Walker)HymenopteraEulophidae[44]
Peribaea tibialis (Robineau-Desvoidy)DipteraTachinidae[44]
Perilampus neglectus BoučekHymenopteraPerilampidae[44]
Perilampus ruficornis FabriciusHymenopteraPerilampidae[44]
Phobocampe lymantriae GuptaHymenopteraIchneumonidae[44]
Phobocampe unicincta (Gravenhorst)HymenopteraIchneumonidae[44]
Pimpla disparis ViereckHymenopteraIchneumonidae[44]
Pimpla rufipes (Miller)HymenopteraIchneumonidae[44]
Pimpla turionellae (L.)HymenopteraIchneumonidae[44]
Pronotalia carlinarum (Szelényi and Erdös)HymenopteraEulophidae[44]
Protapanteles fulvipes (Haliday)HymenopteraBraconidae[44]
Protapanteles liparidis (Bouché)HymenopteraBraconidae[44]
Protapanteles nigerrimus (Roman)HymenopteraBraconidae[44]
Senometopia separata (Rondani)DipteraTachinidae[44]
Siphona boreata MesnilDipteraTachinidae[44]
Tachina magnicornis (Zetterstedt)DipteraTachinidae[44]
Tachina praeceps MeigenDipteraTachinidae[44]
Telenomus embolicus KozlovHymenopteraScelionidae[44]
Telenomus laevisculus (Ratzeburg)HymenopteraScelionidae[44]
Telenomus longistriatus KozlovHymenopteraScelionidae[44]
Telenomus lymantriae KozlovHymenopteraScelionidae[44]
Telenomus macroceps SzabóHymenopteraScelionidae[44]
Telenomus phaIaenarum NeesHymenopteraScelionidae[44]
Telenomus tetratomus (Thomson)HymenopteraScelionidae[44]
Tetrastichomyia clisiocampae AshmeadHymenopteraEulophidae[44]
Tetrastichus sp.HymenopteraEulophidae[44]
Theronia atalantae (Poda)HymenopteraIchneumonidae[44]
Torymus anastativorus FahringerHymenopteraTorymidae[44]
Tyndarichus kuriri FahringerHymenopteraEncyrtidae[44]
Tyndarichus navae HowardHymenopteraEncyrtidae[44]
Zenillia libatrix (Panzer)DipteraTachinidae[44]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Boukouvala, M.C.; Kavallieratos, N.G.; Skourti, A.; Pons, X.; Alonso, C.L.; Eizaguirre, M.; Fernandez, E.B.; Solera, E.D.; Fita, S.; Bohinc, T.; et al. Lymantria dispar (L.) (Lepidoptera: Erebidae): Current Status of Biology, Ecology, and Management in Europe with Notes from North America. Insects 2022, 13, 854. https://doi.org/10.3390/insects13090854

AMA Style

Boukouvala MC, Kavallieratos NG, Skourti A, Pons X, Alonso CL, Eizaguirre M, Fernandez EB, Solera ED, Fita S, Bohinc T, et al. Lymantria dispar (L.) (Lepidoptera: Erebidae): Current Status of Biology, Ecology, and Management in Europe with Notes from North America. Insects. 2022; 13(9):854. https://doi.org/10.3390/insects13090854

Chicago/Turabian Style

Boukouvala, Maria C., Nickolas G. Kavallieratos, Anna Skourti, Xavier Pons, Carmen López Alonso, Matilde Eizaguirre, Enrique Benavent Fernandez, Elena Domínguez Solera, Sergio Fita, Tanja Bohinc, and et al. 2022. "Lymantria dispar (L.) (Lepidoptera: Erebidae): Current Status of Biology, Ecology, and Management in Europe with Notes from North America" Insects 13, no. 9: 854. https://doi.org/10.3390/insects13090854

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop