People and the Gypsy Moth:

Transcription

1 People and the Gypsy Moth: A Story of Human Interactions with an Invasive Species An insight into the introduction, the impact on the environment, and various attempts at controlling the devastation caused by the gypsy moth. Ronald M. Weseloh T hroughout history, people have accidentally or purposefully introduced species of plants or animals to areas outside their natural range. Some such introductions have failed, but often they succeed; and the organisms surviving in the new areas are termed exotic. An exotic species that spreads to new areas, particularly if it has a tendency to spread rapidly, is called invasive. A species that negatively affects the human environment (a pest) can cause many problems. It is no wonder that exotic, invasive pests are the most important ecological competitors of humans on earth. Given the long experience people have had with such organisms, it would seem that effective methods for dealing with them would have been developed already. To a certain extent, this is true. Methods for intercepting potential pests at transportation centers can be effective if pursued vigorously. Incipient outbreaks can be identified, delineated, and eradicated; but some organisms still elude detection and eradication. Given the period of human interaction with these organisms, it seems to me that much can be learned from history. In this article, I consider the case history of an exotic, invasive pest that has had a large human impact the gypsy moth, Lymantria dispar L. (Fig. 1). Among invasive species, the gypsy moth is very conspicuous. It causes economic damage by killing trees it has defoliated. It can be a direct nuisance, crawling over houses and yards and stripping foli180 age from trees. Its populations vary between very high and very low numbers, so its impact varies enormously in time and space, as do people s reactions. Also, the gypsy moth story may be complete, and good documentation exists from the first accidental release to recent unanticipated control. The gypsy moth is in the family Lymantriidae, whose species feed mainly on trees (see Schaefer 1988, for a more complete description of this family). The lymantriids are worldwide in distribution, and the fauna in Europe and Asia are more diverse than in North America. Characteristics that many species have in common include nonfeeding, diurnally active adults; a tendency toward flightless females with reduced wings; sexual dimorphism; and hairy caterpillars, which may have urticating hairs. Fig. 1. Gypsy moth larva. AMERICAN ENTOMOLOGIST Fall 2003

2 The gypsy moth shares many of these characteristics. It is indigenous to Europe and Asia. Females have fully developed wings; the European species are not capable of sustained flight; however, in Asia, females do fly readily, sometimes for several kilometers. In Europe and Asia, gypsy moth outbreaks mainly result in local defoliation. The pest is polyphagous, feeding especially on various species of oaks. Under outbreak conditions, foliage of almost every tree in a forest may be stripped. There is only one generation per year, and eggs are the overwintering stage. Eggs hatch in early spring at the time when leaves of forest trees are just expanding from buds. The larvae complete development over the next two months and then pupate for about two weeks, after which adults emerge. Neither males nor females eat, and after reproducing, both die. Accidental Introduction There is accurate information about how the gypsy moth was introduced into North America. A French artist named Léopold Trouvelot living in Medford, Mass., brought live gypsy moth egg masses back from France in the late 1860s (see Liebhold et al for interesting details of this story). The evident reason was to interbreed gypsy moths with native silk moths so as to produce a variety of silkworm that was not susceptible to the microsporidian, Nosema bombycis Naegeli. Despite Trouvelot s naiveté that lead to this attempt, he was very interested in science and a member of the Boston Society of Natural History (Liebhold et al. 1989). He also devoted a good deal of time to developing mass-rearing techniques for the native polyphemus moth, Antheraea polyphemus (Cramer). In 1868 or 1869, some gypsy moths escaped from the room in his home where he was rearing them. To his credit, Trouvelot reported this incident. Thus, he must have been aware of the implications of such an accidental release. Very shortly afterward, Trouvelot gave up his studies in entomology and became a quite successful astronomer. He returned to France in 1882 and died in 1895 (Liebhold et al. 1989). Initial Impacts and Control Meanwhile, the gypsy moth survived at inconspicuous levels in the nearby woodlands. The insect first became troublesome about 12 years after its introduction in the immediate area surrounding the Trouvelot house. As detailed by Forbush and Fernald (1896), massive numbers of the pest stripped trees of leaves and covered fences, houses, sidewalks, and people. Most of the households in the area had yards with fruit trees and vegetable gardens; and when numbers of the pest were high, these were regularly decimated. Residents were upset by the extreme nuisance caused by the insects and the loss of foliage and death of trees. Homeowners expended a great deal of energy collecting larvae and eggs and destroying them, usually by burning. Despite this devastation, little or no government intervention occurred for about 10 years, probably because the infested area was small (mainly along the street on which the original release occurred) and because the insect was assumed to be native. By 1889, however, the gypsy moth population had built up to a high enough density that it became apparent over a much wider area, about 359 square miles (Burgess and Baker 1938). Perhaps more importantly, the gypsy moth was identified in 1889 as an exotic insect from Europe. An exotic insect in a restricted area can conceivably be eradicated, but only through coordinated, consistent action. Thus, the involvement of government is usually essential, and this was finally recognized. In 1890, the state of Massachusetts appropriated money to attempt eradication of the gypsy moth. Control work began slowly, but in 1891 a definitive survey was carried out that delineated the extent of the infestation (Howard 1897). Early pest control was heavy-handed and labor-intensive compared with that of today. It consisted mainly of destroying egg masses, spraying larvae with arsenical poisons, and placing burlap strips on trees under which larvae would gather and could be later destroyed. Egg masses were first scraped off trees and burned. Burning over the ground destroyed masses on the forest floor, but because intense heat was needed, this was often not good enough. Quoting from Howard (1897), experiments were made with crude petroleum, spraying it over the ground and igniting it, but this was not perfectly effective.a remarkable apparatus was constructed to distribute inflammable oil in a spray which developed wonderful combustive powers. Later in the 1890s, creosote was used to kill egg masses, but still burning over the ground was combined with clearing brush and thinning trees to destroy the pest. All egg masses in trees were routinely destroyed, including those at the tops. For direct control of larvae, Paris green, an arsenical poison, was sprayed on trees. Unfortunately, the concentration of material that killed larvae was often high enough to scorch foliage (Kirkland 1905). The reaction of the public to these control measures varied. Even though controls must have greatly affected the environment, there appeared to be little opposition to the process of burning and clearing perhaps because most operations occurred in woodlands rather than on homeowner s properties. Also, brush removal and tree thinning were considered land improvement techniques. (Unmanaged woodlands were often known as waste lands ; Forbush and Fernald 1896). When trees were burlapped, tree holes and fissures were plugged so larvae would not rest in them. The writer has seen many trees whose lives were undoubtedly saved by this sanitary treatment by the gypsy moth workmen, wrote Howard (1897). However, no doubt due to its tendency to burn vegetation Considerable opposition to the use of Paris green for spraying was manifested by many people living in the infested towns. A mass meeting of opponents of the spraying AMERICAN ENTOMOLOGIST Volume 49 Number 3 181

3 The gypsy moth biological control program mainly involved importing, rearing, and releasing insect parasitoids from Europe and Japan was held in Medford. One citizen, who attempted to cut the hose attached to one of the spraying tanks, and threatened with violence the employees of the Board who had entered upon his land, was arrested and fined. Others neutralized the effects of the spraying by turning the garden hose upon trees and shrubs that had been sprayed, and washed off the solution. The opposition to the spraying affected the results of the work unfavorably to a considerable extent. Forbush and Fernald (1896) in White et al. (1981). This opposition evidently did not persist after lead arsenate was developed for gypsy moth control, probably because at effective dosages, it did not burn foliage. The entire program was coordinated by the state of Massachusetts and included surveys for gypsy moth life stages and follow-up control measures. The expended effort was considerable; the amount of labor and materials amounted to about $200,000 (~$4.0 million current dollars) per year (Marlatt 1905). Such funds had to be appropriated by the state legislature each year. Until 1897, appropriations often were not made soon enough to start control operations in May when they were needed (Howard 1897). By the late 1890s, however, the control program was successful enough that Howard (1897) considered extermination to be possible. In 1900, the Massachusetts State Legislature became convinced that the gypsy moth was no longer a problem, and the program was terminated. From its inception, this first control program against the gypsy moth was aimed at eradication. This is evident from the large, vigorous, and coordinated attack on the pest that was undertaken. The process appeared to have had a reasonable probability of succeeding because The infestation was limited in extent to a location with a well-developed urban infrastructure. The stages of the insect are conspicuous so that infested areas could be readily delimited. The pest spreads slowly, probably because females do not fly. The extreme nuisance nature of the pest guaranteed that elected officials would stay focused on the problem as long as any noticeable defoliation occurred. Taking all of this into account, why was the program stopped? Certainly the experts knew that the insect had not been eradicated by Marlatt (1905) reported that from 1900 to 1902 very little damage occurred; but some defoliation was present, and caterpillars were conspicuous in some areas. For 1903 and 1904, Marlatt (1905) estimated that as much as $200,000 had been spent in local control of the gypsy moth. He also noted that an infestation was found in Providence, R.I., in Most likely, the state program was discontinued because of very low gypsy moth populations in the late 1890s. At low numbers, the gypsy moth is practically invisible; and without a public outcry, the members of the legislature probably saw no reason to spend more money on the pest. With the benefit of hindsight, this was, of course, a mistake. By , the gypsy moth had greatly expanded its range; and by 1905, more than 2,224 square miles were infested (Burgess and Baker 1938). Paradoxically, the gypsy moth might not be present in North America today if it had stayed conspicuous in The low population points have probably been more important to its persistence than the high points, because the low points encourage us to ignore the pest. Early 20th Century By 1905, extermination of the gypsy moth was no longer considered, and the emphasis shifted to containment and control. This emphasis continued through the 1940s. In 1905, for the first time the Federal Government became involved in gypsy moth control, probably because of infestations in another state (Rhode Island). Now that eradication was abandoned, Massachusetts and the U.S. Department of Agriculture (USDA) began a large biological control project. Biological control at that time would have been seen as a desirable approach. The spectacular control of the cottony cushion scale, Icerya purchasi Maskell, on California citrus by the vedalia beetle, Rodolia cardinalis (Mulsant), starting in 1889 (Doutt 1964), was well known to the federal and state gypsy moth workers. The gypsy moth biological control program mainly involved importing, rearing, and releasing insect parasitoids from Europe and Japan (Howard and Fiske 1911, Burgess and Crossman 1929). The guiding philosophy was to establish in North America all of the primary parasites attacking the gypsy moth in Europe (Howard and Fiske 1911). At least 47 natural enemies were imported and released between 1905 and 1929 (Burgess and Crossman 1929). Many of these were extensively reared before release. The program lasted until 1933, not counting a hiatus due to World War I from 1915 to 1921 (Hoy 1976). Such a large effort was unprecedented. Undoubtedly, the motivation for this program was the extreme pest and nuisance nature of the insect, the public outcry against it, and its continuing spread. By 1933, nine natural enemies had become established in North America. These ranged from small hymenopterous egg parasitoids to tachinid flies that attack large larvae (Fig. 2) to a predacious beetle, Calosoma sycophanta L., that feeds on larvae and pupae (Hoy 1976). In almost all cases, the predator and parasitoids became established within a year or two of their release (Hoy 1976). Although the intent was to establish as many natural enemies as possible, the receiving laboratory near Boston was nevertheless sealed to prevent the escape of obviously undesirable organisms such as hyperparasitoids (Burgess and Crossman 1929). Despite the shotgun approach, most of the natural enemies that became established are quite specific 182 AMERICAN ENTOMOLOGIST Fall 2003

4 to the gypsy moth and have had little impact on other organisms. An exception may be the tachinid fly Compsilura concinnata (Meigen). This natural enemy has a very wide host range, and recently, it has been reared from the caterpillars of rare and endangered Lepidoptera (Boettner et al. 2000). The early program did not generally involve the importation of disease agents, but Howard and Fiske (1911) mention that as early as 1907, gypsy moths in North America were dying from a wilt disease (now known to be caused by a baculovirus) that must have arrived in the United States accidentally. Also, in , a fungus pathogen (now thought to be Entomophaga maimaiga Humber, Shimazu, and Soper) that attacks the gypsy moth was imported from Japan. Infected caterpillars were released near Boston, but there is no evidence that the fungus became established at that time (Speare and Colley 1912) (Fig. 3). Despite these efforts, the gypsy moth was still a problem and continued its spread into Rhode Island, Connecticut, western Massachusetts, New Hampshire, and Maine. To check this spread, in 1924, a barrier zone (~ 50 km) was established that extended from Long Island Sound to the Canadian border, roughly along the eastern boundary of New York State. Any infestations of the gypsy moth found in or west of this zone were to be eradicated. The techniques used were those already mentioned: scouting, applying creosote to egg masses, clearing brush, thinning trees and burning over the ground. Burlap flaps were also used, and larvae were sprayed with lead arsenate. (Burgess and Baker 1938). This barrier zone was maintained, with some shifts in location and commitment, until the 1960s (Liebhold et al 1992). During this time, the gypsy moth spread much more slowly than it had before 1916 and after 1965 (Liebhold et al. 1992). Therefore, the zone may have been somewhat effective. During the depression years in the 1930s, large numbers of men in the Citizen Conservation Corps worked to maintain the barrier zone and eradicate isolated infestations beyond it. People still reminisce about their participation in this project. Again, the conspicuous nature of the gypsy moth s damage and its extreme nuisance value guaranteed a strong response on the part of the government. The DDT Era After World War II, the relationship between people and the gypsy moth changed dramatically because of two factors: DDT and practical aerial spraying. At 1 kg/ha aerially applied, DDT was convenient, economical, and effective at controlling the gypsy moth. It seemed like a panacea. Biological control work was dropped. In 1949, an attempt was made to eradicate the gypsy moth on all of Cape Cod, Mass. Essentially the whole area, 93,000 ha, was sprayed that summer, after which surveys delimited areas to be sprayed in the future. Nantucket Island was sprayed in 1951 and Martha s Vineyard in The program lasted at least until 1961 (Dowden 1961). Also in the 1950s, AMERICAN ENTOMOLOGIST Volume 49 Number 3 Fig. 2. Gypsy moth natural enemies purposefully imported and established. From clockwise top left: Anastatus disparis Ruschka, Ooencyrtus kuvanae (Howard), Comsilura concinnata (Meigen), Blepharipa pretensis (Meigen), Brachymeria intermedia (Nees), Cotesia melanoscelus (Ratseburg). large, isolated gypsy moth infestations in Pennsylvania and Michigan were apparently eradicated by aerial spraying of DDT (O Dell 1958). It is not surprising that from at least 1949 through 1957, there was renewed discussion among state and federal authorities about eradicating the pest (Perry 1955, O Dell 1958, Brown 1961). This was, however, never fully undertaken. Even in 1953, there was expressed reluctance of a number of States to undertake an eradication program because of perceived practical difficulties (Perry 1955). A plan was agreed upon to maintain the barrier zone (Perry 1955), presumably so the eradication option would not be lost in the future. This plan was put into effect in 1956, with spraying in areas west of the barrier zone. In 1957, much more spraying was also done in eastern New York and New England (O Dell 1958), but this was really the beginning of the end of the DDT era. In 1957, residues of DDT began to be found on crops and in milk and eggs (Brown 1961). Public opposition to spraying increased in 1962, when Rachel Carson published Silent Spring (Carson 1962). As a consequence, DDT was phased 183

5 Fig. 3. Gypsy moth pathogens. Top: Caterpillar dead from nuclear polyhedrosis virus, Bottom: Dead caterpillar containing resting spores of the fungus, Entomophaga maimaiga Humber, Shimazu & Soper. A significant research development made possible by laboratory rearing has been the discovery and use of the gypsy moth sex pheromone. 184 out of cooperative gypsy moth control programs by 1963, and the insecticide carbaryl was substituted (White et al. 1981). The DDT gypsy moth era lasted little more than 12 years, even though the Environmental Protection Agency did not cancel most uses of the pesticide until 1972 (White et al. 1981). It is not surprising that the demise of DDT for gypsy moth control occurred long before the chemical was actually banned for general use. As I have already pointed out, the gypsy moth is more than a forest defoliator. It also can become extremely abundant on trees in semiforested suburban areas, which are abundant in the northeastern United States. Effective areawide aerial spraying means that infested areas in the suburbs must be sprayed, especially if eradication of the pest is attempted. This was often done without the consent of affected landowners, a kind of eminent domain approach that enraged many people. After residues of DDT were found in foods, it is no wonder that support for mandatory DDT spraying, as would be necessary in any coordinated control program, decayed rapidly. Ironically, the tendency of the gypsy moth to invade private property, which is one factor leading to pressure to control it, also helped lead to the demise of the most effective control method known at the time. Modern Research and Control Until the mid 1960s, little progress beyond what occurred before World War II was made in gypsy moth research. This was partly because of the spectacular successes of the new organic insecticides, but also because there was no practical method for rearing the insect in the laboratory. This changed in 1966 when Leonard and Doane (1966) and O Dell and Rollinson (1966) developed artificial wheat germ-based diets. Now it was possible to rear large quantities of the insect throughout the year, which led to greatly expanded research on many fronts. The driving force for this research was the usual one the desire to control the gypsy moth. But in addition, environmental concerns became much more important. Such concerns were not new, as the early history of the moth indicates; but after Silent Spring, the deleterious effects of insecticides became widely perceived, and much research was aimed at finding alternatives to insecticide controls for the gypsy moth. One fruitful line of research was the development and use of pathogens in sprays to control the pest. Two paths were pursued. In the first, strains of the bacterial pathogen Bacillus thuringiensis Berliner (Bt) were selected through the 1970s and 1980s that were much more lethal to the gypsy moth than any available before. New formulations were also used, and the product was extensively developed by a number of companies until it became the method of choice for controlling the pest (Dubois 1981, Dubois et al. 1993). Because of its specificity to moths and butterflies, it was also generally acceptable to environmentalists. However, in recent years, the concern for preserving rare and endangered Lepidoptera has put pressure on managers to stop using the pathogen. The second path uses the gypsy moth nuclear polyhedrosis virus (a baculovirus) that evidently was introduced accidentally with the gypsy moth. This virus is very specific for the pest and, thus, is environmentally safe. It naturally causes epizootics that result in pest population crashes after two or three years of outbreaks (Doane 1976); however, even now it can only be produced en masse by rearing in live gypsy moths. This has considerably handicapped its commercial development as a spray. Nevertheless, the USDA Animal and Plant Health Inspection Service and the Forest Service have researched practical ways of using the virus in the form of a biological insecticide and the pathogen was registered with the Environmental Protection Agency in 1978 as Gypchek. In forest tests, Gypchek has adequately controlled the gypsy moth (Lewis and Yendol 1981), but the lack of commercialization and the need to rear it on living insects has limited its use to experimental studies. A significant research development made possible by laboratory rearing has been the discovery and use of the gypsy moth sex pheromone. As with many Lepidoptera and other insects, the female gypsy moth produces a pheromone that attracts males for mating. Moths can be attracted to traps baited with this powerful attractant, even AMERICAN ENTOMOLOGIST Fall 2003

6 though there are no other indications of pest presence in an area. The pheromone was known to exist in the early 1900s, and tips of female abdomens were extracted in organic solvents to provide pheromone that could be used in trapping surveys as early as 1932 (Brown and Sheals 1944). Inscoe and Plimmer (1981) recount the history of pheromone research. In the late 1950s, an effort was made to determine the structure of the gypsy moth sex pheromone. In 1960, Jacobson and colleagues discovered what they called gyptol and announced this as the gypsy moth pheromone. Unfortunately, synthesized preparations of gyptol and a related compound gyplure failed to be attractive in the forest. In 1970, Bierl and colleagues announced the discovery of cis-7,8-epoxy-2- methyloctadecane and named it disparlure. This indeed turned out to be very attractive to gypsy moth males in the forest. In the mid-1970s, it was found that the (+) enantiomer of disparlure is the active form (Inscoe and Plimmer 1981). The most effective use of disparlure is as a survey tool. Placed in inexpensive traps that can be left unattended during the flight season of the male moth, disparlure has lead to the detection and delimitation of many isolated infestations of the gypsy moth outside a generally infested area. These areas could then be targeted for eradication. Without our discovery of this pheromone, the gypsy moth might well have a much larger range in North America than it currently does. Disparlure also has been used to control gypsy moths directly through the confusion or mating disruption method. The idea is to saturate a forest environment with synthetic pheromone so that males cannot find females and therefore cannot mate with them. Such a strategy works best when populations of the moths are low, so it seems to be a good method for eradicating isolated infestations. In addition, there have been no environmental problems with the pheromone s use. Disruption trials have been done since Up until 1989, it was usually possible to demonstrate that mating disruption occurred in areas treated with the pheromone, but because moth populations were naturally very low, it was not possible to show population decline. In the 1990s, possibly because of the development of slow-release pheromone dispensers and better evaluation methods, it became possible to show actual population reduction due to pheromone treatment. Indeed, the method can now be used operationally and is most effective when used against isolated, low-level populations (Reardon et al. 1995). Another possible control measure developed during the mid-1960s was the application of the sterile male technique to the gypsy moth. This procedure had been developed and successfully used against the screwworm fly, Cochliomyia hominivorax (Coquerel) in the 1950s (Baumhover et al. 1955). The idea was to release large numbers of males sterilized by radiation so that most females would mate with them rather than native males and so produce sterile eggs. The method became feasible for testing with the gypsy moth when it was possible to raise large numbers of insects in the laboratory. Tests carried out in the 1970s and 1980s demonstrated feasibility. Especially attractive was the possibility of induced sterility, in which male moths were given a sub-sterilizing dose of radiation. When they mated with normal females, the resulting progeny were all sterile. Eggs of the F 1 sterile progeny could be stockpiled and released in the spring to provide overwhelming numbers of sterile males when they matured. Unfortunately, the use of such eggs never really worked. The most effective procedure was the direct release of sterilized or sub-sterilized males. Because of variable efficacy, high cost, and limited production of moths, the method has not been used operationally (Reardon and Mastro 1993). The demise of DDT, the resulting abandonment of eradication attempts, and heightened concern for the environment led to a resurgence of an old development biological control. In the late 1960s, the spread of gypsy moths into new areas in New Jersey and Pennsylvania led these states to set up biological control laboratories to introduce the natural enemies already established in North America and to possibly introduce others from overseas. The USDA again began importing and releasing natural enemies. The emphasis in the 1970s was to release a variety of new natural enemies, particularly parasitoids rather than pathogens or predators; however, few natural enemies became established through this effort. One may have been Brachymeria intermedia (Nees), a chalcid parasitoid of lepidopterous pupae. B. intermedia was imported and released in the early 1900s, but evidence of its definite establishment did not occur until 1967 (Hoy 1976). Schaefer et al. (1989) determined the polyphagous ichneumonid pupal parasitoid Coccygomimus [Pimpla] disparis (Viereck) to be established by The contrast between the lack of success in the new biological control program compared with the old may be due to host specificity. Almost all of the early established natural enemies were host-specific and needed only the gypsy moth to survive. Most of the early enemies did not become established; and those that were imported more recently need unavailable alternative hosts to survive the winter in North America. An exception is the previously mentioned tachinid parasitoid Comsilura concinnata, which has a wide host range among Lepidoptera and rapidly became established even beyond the gypsy moth s range. Unfortunately, this parasitoid is so nonspecific that it also parasitizes rare and endangered Lepidoptera. Recently, Boettner et al. (2000) found that C. concinnata caused mortalities of more than 80% in artificially exposed, native saturniid moth larvae. The recently established C. disparis (Vierect) also has a large host range. The possible deleterious effects of such generalists have not been lost on environmentalists, who use them as examples in attempts to curtail or restrict biological control efforts. Such pressure has Tests carried out in the 1970s and 1980s demonstrated feasibility. Especially attractive was the possibility of induced sterility, in which male moths were given a sub-sterilizing dose of radiation. AMERICAN ENTOMOLOGIST Volume 49 Number 3 185

7 An important development that grew partly out of the new biological control program and the demise of DDT has been the increased number of population and ecological studies on the gypsy moth. lead to recent, healthy reevaluations of biological control practice. More consideration is now given to the possible unintended harm that exotic natural enemies may cause to native flora and fauna. An important development that grew partly out of the new biological control program and the demise of DDT has been the increased number of population and ecological studies on the gypsy moth. Researchers have always been fascinated, as well as frustrated, by the extreme differences in gypsy moth populations during outbreak and latent periods. In the early biological control program, attempts were made to understand the mortality factors that were most important for the gypsy moth. The results were usually superficial, often consisting of presentations of tables of percentage of parasitism and statements that such data shows clearly that this parasite [Blepharipa pratensis (Meigen) in this case] is of great importance in the lightly-infested areas along the border as well as in heavy infestations in the older areas (Burgess and Crossman 1929, p. 76). As far as I am aware, the first in-depth investigations of gypsy moth population ecology were those of Bess (1961). His findings about instarspecific mortality and the hint that small mammals may be important predators were seminal. The work of Campbell in the 1960s and 1970s expanded on this work. Using exclusion experiments, Campbell showed how important birds and mammals are as predators of gypsy moths (Campbell and Sloan 1976, 1977a, b). He also investigated stage-specific mortality (Campbell 1967) and developed a theory to explain the outbreak cycle of the gypsy moth in which mainly small mammals keep populations low until a disturbance causes an increase in moth populations beyond the point where such predation is effective (Campbell 1976, Campbell and Sloan 1978). Elkinton and colleagues have since quantified many of these concepts and shown the important effect that small mammals have in restraining gypsy moth population increases (Elkinton and Liebhold 1990, Elkinton et al.1988). Elkinton et al. (1996) and Jones et al. (1998) go further and show how the variation in abundance of acorns in the forest affects populations of small mammals, which then affect gypsy moth numbers. The Elkinton group also has investigated the influence of parasitoids (Ferguson et al. 1994, Gould et al. 1990) and viruses (Woods and Elkinton 1987, Dwyer and Elkinton 1993) and has pioneered the use of geostatistics in gypsy moth research (Liebhold et al. 1991, 1993; Gribko et al. 1995). Modern attempts also have been made at areawide gypsy moth control and to limit the spread of the pest. These have usually been coordinated Federal State programs. As already mentioned, pheromone trapping is used to locate isolated infestations, which are then systematically eliminated by treatments, usually by spraying B. thuringensis. This strategy was put to severe tests when gypsy moths from Asia were discovered in Washington and Oregon in 1991 and North Carolina in Because females from Asia fly, should these moths ever become established, they probably would spread much faster than the European moths have done. Extensive control measures were carried out, along with intensive surveying reminiscent of the early 1900s to eradicate these moths. Fortunately, the efforts seem to have worked, and Asian gypsy moths are not now established in North America as far as is known. Large-scale projects were carried out in the 1970s, 1980s, and 1990s to better understand the gypsy moth and control it. A large coordinated research effort that occurred in the 1970s resulted in the publication of a compendium volume on the gypsy moth (Doane and McManus 1981). In the 1980s, the Maryland Integrated Pest Management (IPM) Gypsy Moth Project encouraged the development of survey techniques, pathogenic insecticides, and sterile male and pheromone confusion technique controls (Reardon et al. 1993). From 1988 to 1992, the Appalachian IPM Program continued and expanded these projects and was intended to control high and low gypsy moth population levels in the southern leading edge of gypsy moth invasion. Since 1993, a project called Slow the Spread has been underway to implement practical ways of retarding the spread of gypsy moths into new areas, mainly by managing low-level populations. This program is essentially a barrier zone extending from North Carolina to the Upper Peninsula of Michigan. The extensive use of pheromone traps and sophisticated analyses of data in this project are intended to make it possible to control gypsy moths at very low populations (Sharov et al. 1998). As may be expected with the gypsy moth, these large-scale projects have been motivated as much by politics as by science. Despite environmental concerns, the desire to manage the gypsy moth is still strong. The Gypsy Moth Fungus: A Final Solution? After 100 years of contending with the gypsy moth, the insect still could not be managed adequately. This would probably be the situation today if it were not for a phenomenon that occurred in 1989 the sudden and unexpected appearance in North American gypsy moths of a fungus disease caused by the pathogen Entomophaga maimaiga Humber, Shimazu, and Soper (Andreadis and Weseloh 1990, Hajek et al 1990). (For a review of this pathogen, see Hajek 1999.) Hajek et al. (1990) showed genetically that the fungus originated in Japan. Thus, the pathogen had to have been imported at some time before 1989 into North America. The first intentional importation of the fungus occurred early in the 1900s. G. P. Clinton, a plant pathologist from the Connecticut Agricultural Experiment Station was engaged in the spring of 1908 in Massachusetts to do preliminary investigations on the fungus that was decimating the brown-tail moth in New England. With funds made available through the generosity of a friend of Harvard University (Speare and Colley 1912), Clinton was 186 AMERICAN ENTOMOLOGIST Fall 2003

8 sent to Japan in 1909 specifically to collect gypsy moth larvae known to be infected with a fungus disease there. He succeeded in bringing back two infected larvae, from which it was possible to infect others. In 1910 and 1911, infected caterpillars were released around the Boston area, but there was never any evidence that the fungus became established (Speare and Colley 1912). Hajek released a new import of the fungus from Japan in western New York in 1985 and northern Virginia in 1986, but again there was no evidence of establishment. When the fungus became abundant in 1989, the area of infection did not include the sites in New York or Virginia (Hajek 1999). Rather, the center of the infection was Connecticut (Weseloh 1998). Assuming the fungus was established before 1989, it is easy to understand why it became abundant that year. This fungus can only be transmitted under very humid conditions, and the conditions in 1989 were more favorable than at any time since 1920 in Connecticut (Weseloh 1998). Also, the pattern of distribution of the fungus in 1989 in which northern New Jersey, eastern New York, southern Vermont and New Hampshire, and all of Connecticut, Rhode Island, and Massachusetts had infected gypsy moths (Hajek et al. 1995) suggests that the infection started in Connecticut (Weseloh 1998). Hajek et al. (1995) present a careful analysis of how this pathogen may have become established, and they propose five hypotheses: (1) E. maimaiga is native. (2) The fungus became established in and has slowly spread since then. (3) The fungus became established in but only started spreading recently because of a favorable mutation. (4) E. maimaiga was accidentally introduced more recently. (5) The pathogen dispersed naturally from Asia. Hajek et al. (1995) believe that the third or fourth hypothesis is most likely. I favor the fourth because active foreign exploration of gypsy moth natural enemies in China started in 1982 (Schaefer et al. 1984a, 1984b). One site in Northern China where E. maimaiga had been active the same year was examined during that initial trip (personal observation). Although there was no attempt to collect specimens of infected, dead caterpillars, it is possible that some of the long-lived resting spores in the soil could have been inadvertently transported back to the United States. It is perhaps significant that two of the three investigators initially sent to China (W. Wallner and R. Weseloh) live in Connecticut, the center of the distribution of the fungus in Fortunately, E. maimaiga is very specific to the gypsy moth (Hajek et al. 1996). In the years after 1989, it spread rapidly at more than 100 km per year until it infected gypsy moths in all parts of its range (Hajek et al. 1999). The fungus has been a very effective control agent, depressing gypsy moth populations at all density levels (Elkinton et al. 1991). Part of its effectiveness has to do with the longevity of the resistant resting spores. These may remain alive for up to 10 years (Weseloh and Andreadis 2002), thus providing a reservoir of infection that is able to control gypsy moths even at low host densities or under less-than-favorable weather conditions. The advent of E. maimaiga has started another shift in human gypsy moth interactions. Because of this fungus, the pest has become much less noticeable than previously. Outbreaks will probably still happen, but the large potential for dispersal of E. maimaiga and the huge, long-lived reservoir of resting spores in the soil will mean that such outbreaks are likely to be much smaller than they were in the past. Because most research and development on the gypsy moth has occurred because of political pressure, people who used to work on this insect have switched to other invasive pests such as the hemlock wooly adelgid (Adelges tsugae Annand). Perhaps this is appropriate, but a word of caution: we actually know rather little about E. maimaiga. The history of the gypsy moth shows that the pest often surges back when least expected. It would be unwise to ignore either the pest or the pathogen. General Comments Over the long history of human interactions with the gypsy moth, people have responded in predictable ways. Control methods have changed dramatically since the start of the 20th century, yet the motivations for control are the same. When at outbreak numbers, gypsy moths still strip trees of leaves and are still supreme nuisances, and control is a high priority. When the pest is at low numbers, there is essentially no motivation for research and development. Even environmental concerns are not new. People were reacting in modern ways to the spraying of Paris green during the first coordinated control in Massachusetts. The degree of environmental concern has increased, but much of the opposition to control still involves resistance to mandated spraying on private lands. The history of gypsy moth control has been littered with missteps, accidents, good intentions turned wrong, and, fortunately, serendipity. I believe the gypsy moth case is a good example of how careful consideration of the consequences of actions would have made big differences in the outcome. We have to deal with exotic invasive pests. I hope we can do so sensibly. Acknowledgement I thank Joseph S. Elkinton, University of Massachusetts, Amherst, for helpful suggestions on an earlier draft of this manuscript. References Cited Andreadis, T. G., and R. M. Weseloh Discovery of Entomophaga maimaiga in North American gypsy moth, Lymantria dispar. Proc. Nat. Acad. Sci. USA 87: Baumhover, A. H., A. J. Graham, B. A. Bitter, D. E. Hopkins, W. D. New, F. H. Dudley, and R. C. Bushland Screwworm control through release of sterilized flies. J. Econ. Entomol. 48: 462 AMERICAN ENTOMOLOGIST Volume 49 Number 3 187

9 John W. Hock Company Manufacturer of insect flight traps for 28 years P.O. Box 12852, Gainesville, FL (352) (352) fax Bess, H. A Population ecology of the gypsy moth. Conn. Agric. Exp. Stn. Bull Boettner, G. H., J. S. Elkinton, and C. A. Boettner Impact of an introduced biological control on three species of native saturniids. Conserv. Biol. 14: Brown, R. C., and R. H. Sheals The present outlook on the gypsy moth problem. J. For. 42: Brown, W. L., Jr Mass insect control programs: Four case histories. Psyche 68: Burgess, A. F., and W. L. Baker The gypsy and brown-tail moths and their control. U.S. Dep. Agric. Circ Burgess, A. F., and S. S. Crossman Imported insect enemies of the gipsy [sic] moth and the browntail moth. U.S. Dep. Agric. Tech. Bull. 86. Campbell, R. W The analysis of numerical change in gypsy moth populations. For. Sci. Monogr. 15. Campbell, R. W Comparative analysis of numerically stable and violently fluctuating gypsy moth populations. Environ. Entomol. 5: Campbell, R. W., and R. J. Sloan Influence of behavioral evolution on gypsy moth pupal survival in sparse populations. Environ. Entomol. 5: Campbell, R. W., and R. J. Sloan. 1977a. Natural regulation of innocuous gypsy moth populations. Environ. Entomol. 6: Campbell, R. W., and R. J. Sloan. 1977b. Sources of mortality among late instar gypsy moth larvae in the Light Weight Townes Trap Generalist insect collector, especially effective for Hymenoptera and Diptera Very light and mobile, easy to set up and transport Made of sun-resistant polyester and about 2 m in length Complete with tie-down lines and polypropylene wet-anddry collection head sparse populations. Environ. Entomol. 6: Campbell, R. W., and R. J. Sloan Numerical bimodality among North American gypsy moth populations. Environ. Entomol. 7: Carson, R Silent spring. Houghton and Mifflin, Boston. Doane, C. C Ecology of pathogens of the gypsy moth, pp In J. F. Anderson and H. K. Kaya [Eds.], Perspectives in forest entomology, Academic Press, New York, NY. Doane, C. C., and M. L. McManus [Eds.] The gypsy moth: research toward integrated pest management. U.S. Dep. Agric. For. Serv. Tech. Bull Doutt, R. L The historical development of biological control, pp In P. DeBach and E. I. Schlinger [Eds.], Biological control of insect pests and weeds. Reinhold Publishing, New York. Dowden, P. B The persistence of gypsy moth parasites in heavily sprayed areas on Cape Cod, Massachusetts. J. Econ. Entomol. 54: Dubois, N. R Bacillus thuringiensis. U.S. Dep. Agric. For. Serv. Tech. Bull. 1584: Dubois, N. R., R. C. Reardon, and K. Mierzejewski Field efficacy and deposit analysis of Bacillus thuringiensis, Foray 48B, against gypsy moth (Lepidoptera: Lymantriidae) J. Econ. Entomol. 86: Dwyer, G., and J. S. Elkinton Using simple models to predict virus epizootics in gypsy moth populations. J. Anim. Ecol.62: Elkinton, J. S., and A. M. Liebhold Population dynamics of gypsy moths in North America. Annu. Rev. Entomol. 35: Elkinton, J. S., J. R. Gould, A. M. Liebhold, H. R. Smith, and W. E. Wallner Are gypsy moth populations in North America regulated at low density?, pp In W. E. Wallner and K. A. McManus [Eds.], Proceedings, Lymantriidae: a comparison of features of New and Old World tussock moths. USDA Forest Service, Northeast Forest Experiment Station, Broomall, PA. Elkinton, J. S., A. E. Hajek, G. H. Boettner, and E. E. Simons Distribution and apparent spread of Entomophaga maimaiga (Zygomycetes: Entomophthorales) in gypsy moth (Lepidoptera: Lymnatiidae) populations in North America. Environ. Entomol. 20: Elkinton, J.S., W. M. Healy, J. P. Buonaccorsi, G. H. Boettner, A. M. Hazzard, H. R. Smith, and A. M. Liebhold Interactions among gypsy moths, white-footed mice, and acorns. Ecology 77: Ferguson, C. S., J. S. Elkinton, J. R. Gould, and W. E. Wallner Population regulation of gypsy moth (Lepidoptera: Lymantriidae) by parasitoids: Does spatial density dependence lead to temporal density dependence? Environ. Entomol. 23: Forbush, E. H., and C. H. Fernald The gypsy moth, Porthetria dispar (Linn.). Wright and Potter Printing, Boston. Gould, J., J. S. Elkinton, and W. E. Wallner Density-dependent suppression of experimentally created gypsy moth, Lymantria dispar (Lepidoptera: Lymantriidae) populations. J. Anim. Ecol. 59: Gribko, L. S., A. M. Liebhold, and M. E. Hohn Model to predict gypsy moth (Lepidoptera: 188 AMERICAN ENTOMOLOGIST Fall 2003

10 Lymantriidae) defoliation using Kriging and logistic regression. Environ. Entomol. 24: Hajek, A. E Pathology and epizootiology of Entomophaga maimaiga infections in forest Lepidoptera. Micro. Mol. Biol. Rev. 63: Microbiology and Molecular Biology Reviews. Hajek, A. E., R. A. Humber, J. S. Elkinton, B. May, S. R. A. Walsh, and J. C. Silver Allozyme and RFLP analyses confirm Entomophaga maimaiga responsible for 1989 epizootics in North American gypsy moth populations. Proc. Nat. Acad. Sci. USA 87: Hajek, A. E., R. A. Humber, and J. S. Elkinton Mysterious origin of Entomophaga maimaiga in North America. Am. Entomol. 41: Hajek, A. E., L. Butler, S. R. A. Walsh, J. C. Silver, F. P. Hain, F. L. Hastings, T. M. ODell, and D. R. Smitley Host range of the gypsy moth (Lepidoptera: Lymantriidae) pathogen Entomophaga maimaiga (Zygomycetes: Entomophthorales) in the field versus laboratory. Environ. Entomol. 25: Howard, L. O The gipsy [sic] moth in America: a summary account of the introduction and spread of Porthetria dispar in Massachusetts and of the efforts made by the state to repress and exterminate it. U.S. Dep. Agric. Bull. 11, New Series (Div. Entomol.). Howard, L. O., and W. F. Fiske The importation into the United States of the parasites of the gypsy moth and brown-tailed moth. U.S. Dep. Agric. Entomol. Bull. 91. Hoy, M. A Establishment of gypsy moth parasitoids in North America: An evaluation of possible reasons for establishment or non-establishment, pp In J. F. Anderson and H. K. Kaya [Eds.], Perspectives in forest entomology. Academic Press, New York. Inscoe, M. N., and J. R. Plimmer Chemistry of isolation, identification, and synthesis [of pheromone]. U.S. Dep. Agric. For. Serv. Tech. Bull. 1584: Jones, C.G., R. S. Ostfeld, M. P. Richard, E. M. Schauber, and J. O. Wolff Chain reactions linking acorns to gypsy moth outbreaks and Lyme disease risk. Science 279: Kirkland, A. H The gypsy and brown-tail moths. Bulletin 1, Wright & Potter Printing Co., Boston. Leonard, D. E., and C. C. Doane An artificial diet for the gypsy moth Porthetria dispar (Lepidoptera: Lymantriidae). J. Econ. Entomol. 59: Lewis, F. B., and W. G. Yendol Efficacy [of virus]. U.S. Dep. Agric. For. Serv. Tech. Bull. 1584: Liebhold, A., V. Mastro, and P. W. Schaefer Learning from the legacy of Léopold Trouvelot. Bull. Entomol. Soc. Am. 35: Liebhold, A. M., X. Zhang, M. E. Hohn, J. S. Elkinton, M. Tichurst, G. L. Benzon, and R. W. Campbell Geostatistical analysis of gypsy moth (Lepidoptera: Lymantriidae) egg mass population. Environ. Entomol. 20: Liebhold, A. M., J. A. Halverson, and G. A. Elmes Gypsy moth invasion in North America: a quantitative analysis. J. Biogeogr. 19: Liebhold, A. M., R. E. Rossi, and W. P. Kemp Geostatistics and geographic information systems AMERICAN ENTOMOLOGIST Volume 49 Number 3 in applied insect ecology. Annu. Rev. Entomol. 38: Marlatt, C. L Report on the gypsy moth and the brown-tail moth, July, U.S. Dep. Agric. Bur. Entomol. Circ. 58. ODell, T. M., and W. D. Rollinson A technique for rearing gypsy moth, Porthetria dispar (L.), on an artificial diet. J. Econ. Entomol. 59: O Dell, W. V Gypsy moth: introduction, spread, and control efforts in the U.S. Farm Chemicals (Feb.), pp , 44, 53. Perry, C. C Gypsy moth appraisal program and proposed plan to prevent spread of the moths. U.S. Dep. Agric. Tech. Bull Reardon, R. C., and V. C. Mastro Development and status of the sterile insect technique for managing gypsy moth. USDA Forest Service, Appalachian Integrated Pest Management, Technology Transfer NA-TP Reardon, R., L. Venables, and A. Roberts The Maryland Integrated Pest Management Gypsy Moth Project U.S. Dep. Agric. For. Serv. NA-TP Reardon, R. C., D. S. Leonard, V. C. Mastro, B. A. Leonhardt, W. McLane, and S. Talley Using mating disruption to manage gypsy moth: a review. USDA Forest Service, National Center of Forest Health Management, Technology Transfer, FHMNC Schaefer, P. W Diversity in form, function, behavior, and ecology: An overview of the Lymantriidae (Lepidoptera) of the world, pp In W. E. Wallner and K. A. McManus [Eds.], Pro- SANTE TRAPS Makers of Malaise traps and other arthropod collecting devices since Malaise traps (Townes style and the original Malaise style), 2 way Malaise traps Canopy traps Winkler litter extractors Mini-Winkler litter extractors Litter sifters Custom made field cages of all dimensions SANTE TRAPS 1118 Slashes Rd. Lexington, KY Tel. (859) For more information check out our website at or contact us at [email protected] 189

11 ceedings, Lymantriidae: a comparison Of Features of New and Old World tussock moths. USDA Forest Service, Northeast Forest Experiment Station, Broomall, PA. Schaefer, P. W., R. M. Weseloh, X. Sun, W. E. Wallner, and J. Yan. 1984a. Gypsy moth, Lymantria (=Ocneria) dispar (L) (Lepidoptera: Lymantriidae), in the People s Republic of China. Environ. Entomol. 13: Schaefer, P. W., J. Yan, X. Sun, W. E. Wallner and R. M. Weseloh. 1984b. Natural enemies of the gypsy moth, Lymantria dispar (L) (Lepidoptera: Lymantriidae), in China. Sci. Silvae Sin. 20: Schaefer, P. W., R. W. Fuester, R. J. Chianese, L. D. Rhoads, and R. B. Tichenor, Jr Introduction and North American establishment of Coccygomimus disparis (Hymenoptera: Ichneumonidae), a polyphagous pupal parasite of Lepidoptera: including gypsy moth. Environ. Entomol. 18: Sharov, A. A., A. M. Liebhold, and E. A. Roberts Optimizing the use of barrier zones to slow the spread of gypsy moth (Lepidoptera: Lymantriidae) in North America. J. Econ. Entomol. 91: Speare, A. T., and R. H. Colley The artificial use of the brown-tail fungus in Massachusetts. with practical suggestions for private experiment, and a brief note on a fungus disease of the gypsy caterpillar. Wright & Potter Printing Company, Boston. Weseloh, R. M Possibility for recent origin of the gypsy moth (Lepidoptera: Lymantriidae) fungal pathogen Entomophaga maimaiga (Zygomycetes: Entomophthorales) in North America. Environ. Entomol. 27: Weseloh, R. M., and T. G. Andreadis Detecting the titer in forest soils of spores of the gypsy moth (Lepidoptera: Lymantriidae) fungal pathogen, Entomophaga maimaiga (Zygomycetes, Entomophthorales). Can. Entomol. 134: White, W. B., W. H. McLane, and N. F. Schneeberger Pesticides. U.S. Dep. Agric. For. Serv. Tech. Bull. 1584: Woods, S.A., and J. S. Elkinton Bimodal patterns of mortality from nuclear polyphedrosis virus in gypsy moth (Lymantria dispar) populations. J. Invert. Pathol. 50: Ronald M. Weseloh, Department of Entomology, Connecticut Agricultural Experiment Station, 123 Huntington Street, New Haven, Connecticut 06511, has been studying the gypsy moth for 33 years. He recenltly retired and can now be reached at (203) or AMERICAN ENTOMOLOGIST Fall 2003