Biol Invasions (2010) 12:2895–2912 DOI 10.1007/s10530-010-9735-6

ORIGINAL PAPER

Micro-managing invasions: eradication and control of invasive with microbes

Ann E. Hajek • Patrick C. Tobin

Received: 15 May 2009 / Accepted: 23 September 2009 / Published online: 31 March 2010 Springer Science+Business Media B.V. 2010

Abstract Non-indigenous arthropods are increas- arthropod management programs within a general ingly being introduced into new areas worldwide and context, and compare the use of microbes in gypsy occasionally they cause considerable ecological and management with diverse microbes being economic harm. Many invasive arthropods particu- developed for use against other invasive arthropods. larly pose problems to areas of human habitation and native ecosystems. In these cases, the use of Keywords Arthropod pathogens Á environmentally benign materials, such as host-spe- Augmentation biological control Á Biological cific entomopathogens, can be more desirable than invasions Á Classical biological control Á broader spectrum control tactics that tend to cause Containment Á Eradication Á dispar greater non-target effects. The majority of successful eradication programs using arthropod pathogens have targeted invasive with Bacillus thurin- Introduction giensis kurstaki (Btk), such as eradication efforts against the gypsy moth, (L.), in The introduction of non-native arthropods in natural North America and New Zealand. Both Btk and areas such as wetlands and forests is increasing in Lymantria dispar nucleopolyhedrovirus have been frequency due to the relatively recent waves of successfully used in efforts to limit the spread of increased global trade and travel (National Research L. dispar in the United States. For invasive arthropod Council 2002; Work et al. 2005; Brockerhoff et al. species that are well established, suppression pro- 2006; Liebhold et al. 2006; McCullough et al. 2006). grams have successfully used arthropod-pathogenic Some introductions result in the successful establish- viruses, bacteria, fungi and nematodes for either ment of an invasive species that in turn causes short- or long-term management. We will summarize considerable environmental and economic harm to the use of pathogens and nematodes in invasive the functioning and composition of native communi- ties and ecosystems (Parker et al. 1999; Mack et al. 2000; Pimentel et al. 2005). Generally, the invasive A. E. Hajek (&) Department of Entomology, Cornell University, Ithaca, species that receive the most attention are those that NY 14853-2601, USA alter communities and ecosystems, sometimes irre- e-mail: [email protected] versibly, over a geographically broad area. As we increase our awareness and ability to detect new P. C. Tobin USDA Forest Service, Northern Research Station, introductions, more invasive species could be com- Morgantown, WV 26505-3101, USA bated before their inimical effects are irreversible. 123 2896 A. E. Hajek, P. C. Tobin

Efforts to combat invasive species begin with reproducing individual of a species or the reduction of prevention of introduction and establishment. In some their population density below sustainable levels’’ instances, the arrival of a new species is detected early (Myers et al. 2000). Debate on the feasibility of enough to prevent establishment through intervention eradication has been quite contentious in the past strategies (Veitch and Clout 2002; Glare 2009; Hajek (DeBach 1964; Knipling 1979; Carey 1991). Dahlsten and Tobin 2009; Simberloff 2009), or the founder and Garcia (Dahlsten and Garcia 1989) edited a survey population size is insufficient to successfully establish of efforts to eradicate invasive arthropod species and even without use of control tactics (Williamson and plant pathogens and argued that eradication programs Fitter 1996; Simberloff and Gibbons 2004). Numerous were often crisis situations and focused heavily on use countries have developed risk assessments to define of chemical pesticides without adequate knowledge of those species that are known to arrive frequently, pests and systems being treated. Of the 12 eradication mostly due to trade, and that have the potential for programs described in their book, only four were establishment and costly impacts; thus, many detection considered successful. However, the low rate of efforts specifically target these commonly-introduced eradication success does not necessarily argue against invaders arriving along known pathways (Committee attempting eradication if, for example, the benefits of on the Scientific Basis for Predicting the Invasive eradication exceed the costs of the effort (Regan et al. Potential of Nonindigenous Plants and Plant Pests in 2006; Edwards and Leung 2009). the United States 2002). There is also recognition of the While eradication of an unwanted arthropod is importance of ballast water in the introduction of indeed possible (Simberloff 2009), success is only aquatic species and the need to manage this invasion likely under relatively strict conditions (Myers et al. pathway (Ruiz et al. 2000; Drake and Lodge 2004). 2000). General guidelines have been developed pre- The identification of important invasion pathways senting criteria that are necessary for success in and vectors as well as those species likely to be eradication: effective methods for detection and con- introduced help to optimize available, yet usually trol, authority to do what is needed, measures to limited, resources to maintain surveillance programs at prevent reinvasion, and funding, because eradication ports-of-entry. However, given the volume of global campaigns are usually quite costly (Myers et al. 2000). trade and travel, and the fact that only a very small Additional costs would also be required to ecologi- proportion of pathways and vectors are checked, many cally restore the impacted area following an eradica- species still become introduced despite these efforts tion effort (Myers et al. 2000; Hall and Hastings 2007). (Work et al. 2005; Brockerhoff et al. 2006; Liebhold Restoring an ecosystem to the conditions existing prior et al. 2006; McCullough et al. 2006). For example, to establishment of an invasive is difficult, especially Brockerhoff et al. (2006) reported that roughly 10% of when the native flora and fauna present before the shipments entering New Zealand are inspected by invasive established had not been well documented. quarantine officers, while \2% of cargo entering the In the event that eradication efforts are initially not United States is inspected (Work et al. 2005; feasible or become infeasible, the subsequent options McCullough et al. 2006). In addition, some species are to attempt control through containment or pop- are not considered as pests in their native ranges but are ulation suppression, or to do nothing. In general, considerably more problematic when introduced into methods for controlling arthropods have been devel- new regions, such as the emerald ash borer [Agrilus oped for many diverse systems and pests over many planipennis (Fairmaire)] invasion of North America years but, the standard methods have generally (Poland and McCullough 2006) and the targeted pests of managed resources, in particular invasion [Hyphantria cunea (Drury)] of Asia (Gomi agriculture and forestry. However, many of the tactics 2007). Thus, efforts to prevent introductions of only and especially the use of chemical pesticides to known pests can be inadequate. control arthropod pests in managed systems such as If establishment of a non-native arthropod has not agricultural and horticultural crops, are not appropri- been prevented, and a newly established species is ate for use outside of these systems due to pesticide considered to be potentially harmful, then the first label regulations. In natural areas and especially those management approach considered is often eradication. areas that are publicly-owned such as federal- or Eradication is the forced ‘‘removal of every potentially state-managed areas, there are regulations restricting 123 Micro-managing arthropod invasions 2897 pest control practices (e.g., National Environmental using microbes for arthropod control has been exten- Policy Act) due to concerns regarding, for example, sively evaluated and the microbes that are used are the potential for non-target effects and toxicity to predominantly very host specific (Hajek 1999; humans and wildlife. These regulations can prohibit Hokkanen and Hajek 2003; O’Callaghan and the use of broad spectrum tactics, such as use of Brownbridge 2009), especially in comparison with chemical pesticides. Moreover, in urban areas, there most chemical insecticides. can be considerable human objection to any man- In this review, we will first present successful agement interventions against invasive arthropods examples of the use of a microbial biopesticide to (e.g., East Bay Pesticide Alert 2009), which increases eradicate non-native arthropod species. We will then the need for environmentally benign tactics. Thus, focus on the use of pathogens and parasitic nema- methods for controlling invasive arthropods must be todes in the management of spread and population tailored for individual ecosystems being impacted by suppression of established non-native invasive arthro- a particular invasive species and, depending on the pods. In particular, management efforts aimed at area, tactics often must be environmentally benign. eradicating, containing, and suppressing populations Invasive species are often initially introduced to of the gypsy moth, Lymantria dispar (L.), have relied areas of human habitation where goods and people upon a diversity of types of pathogens, arguably more arrive, so much so that recent studies of invasion risk so than for any other invasive arthropod. We will have incorporated gravity models that were applied describe the microbes that have been developed for historically to understand the movement of humans use against the gypsy moth and draw comparisons and their goods (Bossenbroek et al. 2001; Leung et al. with the development of microbes against A. glab- 2004; Leung and Mandrak 2007). Initial efforts to ripennis and A. planipennis, which were detected in eradicate an unwanted invader tend to be conducted North America in 1996 and 2002, respectively. where it was first detected, often assumed (but not always correctly) to be where the species was first introduced. Examples include the efforts to eradicate Eradication Asian longhorned beetle, Anoplophora glabripennis (Motschulsky) in New York City and Chicago (Hu Eradication is the forced and complete removal of a et al. 2009), and emerald ash borer, A. planipennis,in species from a geographic area, and as such, can be a Detriot (Poland and McCullough 2006). The feasi- very difficult and costly undertaking. Generally, bility of undertaking eradication is often assessed eradication is more likely to be feasible when the after the infested area has been delimited. If eradi- initial founder population is smaller in abundance and cation is not considered feasible, containment and spatial distribution, or has been detected very early population suppression measures could be undertaken after arrival (Rejma´nek 2000; Lockwood et al. 2007; throughout the distribution of the invasive species Liebhold and Tobin 2008). Measuring the success of and may continue for many years. Regardless, eradication campaigns against invasive arthropod measures used in the management of invasive pests can be challenging, a fact perhaps best exem- arthropods must limit human health effects and plified by the long-standing debate on the eradica- impacts to non-target species. tion, or lack thereof, of the Mediterranean fruit Microbial biopesticides have been used success- fly, Ceratitis capitata (Wiedemann), in California fully in several eradication and containment efforts (Barinaga 1990; Carey 1991, 2008; Headrick and against non-native arthropods (Glare 2009; Hajek and Goegen 1994). In addition, many past eradication Tobin 2009), and a diversity of pathogens, parasites, programs were not reported or summarized and it is and predators have been used to successfully suppress therefore often difficult to know the details of past established populations of invasive arthropod species eradication programs and whether they were success- (Hoddle 2004; Hajek et al. 2007; Tobin and Blackburn ful (Simberloff 2002). 2007). The use of these tactics in eradication, contain- A symposium in 2001 focused on the eradications ment and suppression programs has many advantages of island invasions and a subsequent proceedings over synthetic chemical pesticides which tend to be the summarized [70 reports of various eradication backbone of most arthropod control. The safety of programs (Veitch and Clout 2002). The majority of 123 2898 A. E. Hajek, P. C. Tobin

Table 1 Successful use of Bacillus thuringiensis kurstaki for eradication of invasive Lepidoptera (Glare 2009; Ebata 2009; Gypsy Moth Digest 2009) Invasive lepidopteran species Area of endemism Location of eradication Years of eradication program treatment

Lymantria dispar (L.), Both European and Asian 29 locations in British 1982–2008 Gypsy moth Columbia, Canada Both European and Asian Throughout the United 1980–2008 States (see Table 2) Orgyia thyellina Butler, North Asia Auckland, New Zealand 1996–1997 White spotted tussock moth anartoides Walker, Australia Auckland, New Zealand 2000–2003 Painted apple moth Asian member of the L. dispar species Probably North Asiaa Hamilton, New Zealand 2003 complex, Asian gypsy moth Curiously, all of these species belong to the Family Lymantriidae a The exact identity of the introduced species could never be determined but the best guess was Lymantria umbrosa Butler from Siberia/Japan, a member of the L. dispar species complex. In the New Zealand eradication campaign, this species was commonly referred to as Asian gypsy moth these eradication programs dealt with vertebrates, However, in recent years microbial biopesticides have with a few targeting plants, and even fewer centered been used when appropriate agents are available. For on arthropods. In 2005, a report of European any control tactic to be appropriate for eradication, it eradication programs, mostly after the 1980s, sum- must be able to induce high levels of mortality in the marized 33 programs conducted on islands and four target pest. One such microbial biopesticide, the on the mainland, all directed against mammals with entomopathogenic bacterium Bacillus thuringiensis no eradication efforts against invasive arthropods kurstaki (Btk), has been used extensively to eradicate (Genovesi 2005). Eradications of arthropods appear several invasive lepidopteran species (Table 1), to be undertaken much less frequently than eradica- including the gypsy moth. The gypsy moth nucleo- tions of vertebrates based on such published summa- polyhedrovirus (LdMNPV) has also been used in ries; nevertheless, eradication is still an important gypsy moth eradication programs, but to a lesser strategy used against invasive arthropods, especially extent. We will describe the use of these two pathogens those species predicted to significantly alter ecosys- in eradication attempts against the gypsy moth. tems. For example, Klassen (1989) summarized 42 US eradication programs against arthropod invaders, Use of Btk and LdMNPV for eradication with 21 regarded as successful even though several of the gypsy moth targeted species were reintroduced within 9 years after being successfully eradicated (Myers et al. The gram positive bacterial pathogen Bacillus thur- 1998). ingiensis Berliner (Bt) has been used extensively for Chemical insecticides have historically been the control of Lepidoptera, Diptera, and Coleoptera. As of primary tactic used in many arthropod eradication 2006, 361 Bt products consisting of spores plus toxins programs (e.g., Koyama et al. 1984; Daane and or toxins alone were registered with the United States Wilhoit 1989; Davis and Garcia 1989; Kuba et al. Environmental Protection Agency (Garczynski and 1996; Allwood et al. 2002), including the failed Siegel 2007). Sporangia of Bt carry a spore and a toxin attempt to eradicate the gypsy moth from North crystal and these are ingested by the target . America in the 1890s (Doane and McManus 1981). Different subspecies and strains of Bt carry different Other programs have relied on the sterile male release toxins with differential host specificity. After the toxin technique (Anonymous 1992; Galvin and Wyss 1996; is ingested, lesions occur in the gut of a susceptible Myers et al. 1998), sometimes in combination with host which often dies within 1–2 days (Broderick chemical insecticides (Oladunmade et al. 1986). et al. 2006). Bacillus thuringiensis commonly occurs

123 Micro-managing arthropod invasions 2899 in the soil worldwide, with the spore stage providing scientific concerns over non-target effects, even excellent persistence. This bacterium has also been though Btk can still affect some non-target native isolated from phylloplane samples as well as from Lepidoptera. dead or moribund insect larvae. Curiously, although In areas where there are concerns over non-target Bt is widespread, naturally occurring epizootics are effects, especially in the case of rare and endangered rare except when occur in enclosed environ- Lepidoptera, eradication programs have relied on the ments (Aronson et al. 1986). use of LdMNPV. Lymantria dispar nucleopolyhedro- In recent decades, Bt toxin genes have been virus (LdMNPV) belongs to the Family Baculoviri- inserted into crop plants for pest control (Gould dae, a virus family infecting only arthropods, and 1998). However, for gypsy moth management in principally Lepidoptera. Virions of baculoviruses are North America, the Btk strain HD-1, originally surrounded by a protein matrix which protects them in isolated from the pink bollworm, Pectinophora nature. Early instar gypsy are most susceptible gossypiella (Saunders), is now most commonly used. to LdMNPV, which principally infects through the gut It is mass produced in fermenters, formulated and so virions must be ingested to infect. This virus is applied as aerial or ground sprays. The use of Btk has thought to have been introduced prior to 1907 (Hajek been studied extensively to optimize the amount of et al. 2005). Epizootics can occur in outbreaking material that survives application and infects gypsy gypsy moth populations when transmission is moth hosts (cf. Solter and Hajek 2009). It is always increased due to the disintegration of larval cadavers, applied against the 2nd or 3rd instars, which are the which release viral occlusion bodies onto foliage. most susceptible life stages (Reardon et al. 1994). Occlusion bodies are then ingested by feeding larvae, Because of the effectiveness of pheromone-baited resulting in infection (Elkinton and Liebhold 1990). traps in detecting newly-arrived gypsy moth popula- Unfortunately, LdMNPV cannot be easily mass- tions, many populations can be aggressively and produced because it must be produced in vivo. feasibly targeted for eradication. Prior to the 1980s, Records of gypsy moth eradication projects in the most eradication projects in the United States relied United States date at least to the early 1970s (Gypsy on chemical insecticides such as carbaryl and dylox, Moth Digest 2009), and in almost every year since but Btk has gradually become the dominant tactic then, there have been many eradication programs used in gypsy moth eradication (Fig. 1; Hajek and across the United States (Table 2; Hajek and Tobin Tobin 2009). The transition from more broad spec- 2009). Despite the fact that female gypsy moths in trum chemical insecticides to a more host-specific North America are incapable of flight and early control agent such as Btk reflects increased public and instars are only capable of passive dispersal through ballooning, it is surprising how often L. dispar is

1 introduced from established areas to new areas within the United States. This movement virtually always can be tracked to the movement of humans and their 0.75 goods (Liebhold and Tobin 2006; Hajek and Tobin 2009). Since 1972, there have been 226 eradication projects in 24 states, and in over 60% of these 0.5 programs, Btk (primarily) or LdMNPV have been used (Table 2). The threshold for initiating an 0.25 eradication campaign can sometimes vary, but gen-

Chemical erally, high male moth trap catches or the confirma- Btk tion of other life stages such as egg masses, which are 0 1972 1977 1982 1987 1992 1997 2002 2007 indicative of a reproducing population, trigger an eradication program. Specific gypsy moth eradication Fig. 1 Proportion of acres treated by chemical insecticides or programs that have received considerable attention Btk in gypsy moth eradication programs in the United States, resulted from detection of the Asian strain of 1972–2007. In 1978, there were no eradication projects recorded, and in 2000, the majority of acres were treated with L. dispar in British Columbia, Canada, and Wash- mating disruption tactics (cf. Thorpe et al. 2006) ington and Oregon in 1991, mainly because the Asian 123 2900 A. E. Hajek, P. C. Tobin

Table 2 Number of gypsy Statea Total number Number of eradication Total Area (km2) treated using moth eradication projects in of eradication projects involving area treated the United States, 1972– projects (km2) 2007, and the frequency of Btk LdMNPV Btk LdMNPV projects by state involving Btk and LdMNPV as tactics Alabama 2 0 0 0.2 0.0 0.0 and the respective areas Arizona 4 2 0 709.3 692.1 0.0 treated (Gypsy Moth Digest 2009) California 6 4 0 205.6 167.2 0.0 Colorado 4 2 0 0.2 0.9 0.0 Georgia 5 4 0 178.1 158.9 0.0 Idaho 4 4 0 24.4 24.4 0.0 Illinois 15 12 0 97.7 59.3 0.0 Indiana 18 7 0 109.3 62.2 0.0 Iowa 4 4 0 1.9 1.8 0.0 Kentucky 2 0 0 10.4 0.0 0.0 Michigan 9 3 0 255.3 16.1 0.0 Minnesota 12 8 0 35.7 23.2 0.0 Nebraska 2 0 0 12.9 0.0 0.0 North Carolina 23 20 3 2155.6 1940.6 13.1 Ohio 17 3 1 64.3 14.0 0.6 Oregon 16 14 0 7316.7 7283.4 0.0 South Carolina 7 2 0 10.9 0.3 0.0 South Dakota 5 0 0 0.3 0.0 0.0 Tennessee 14 8 1 858.6 397.8 1.2 a Some states listed were Utah 7 7 0 1156.6 1156.5 0.0 considered part of Virginia 14 3 0 685.0 199.3 0.0 eradication programs for Washington 13 11 0 168.4 154.5 0.0 only a portion of the years listed (i.e., prior to the state West Virginia 4 0 0 71.9 69.5 0.0 becoming part of the Wisconsin 19 15 1 4623.5 4458.2 19.9 established range of gypsy Total 226 133 6 18752.6 16880.0 34.8 moth) strain of gypsy moth is not established anywhere in Although there are Bt endotoxins that are active North America (see Hajek and Tobin 2009). against beetles and flies, at present no combinations of effective strains plus delivery methods have been Use of microbes for eradication of invasive identified that would provide the fast kill of large wood-boring insects percentages of target hosts that would be needed for eradication efforts against, for example, A. glabrip- Products that are used for eradication generally must ennis and A. planipennis. kill large percentages of exposed individuals quickly, hopefully before they reproduce or disperse. Bt fits these characteristics well because it usually kills due Containment to activity of a toxin. Btk has been very appropriate for use against larval Lepidoptera feeding externally For many non-native arthropod species, eradication on leaves, and has been used successfully not only for efforts are not undertaken or are not successful. A eradication of European and Asian gypsy moth in management focus could thus turn to a strategy of North America, but also for eradication of the gypsy containment, which refers to efforts that seek to moth, painted apple moth (Teia anartoides Walker) eliminate or reduce the movement of an invader to and the white spotted tussock moth (Orgyia thyellina areas outside of its established range (Randall 1996; Butler) in New Zealand (Table 1; Glare 2009). Sharov and Liebhold 1998a, b; Rejma´nek 2000; Byers 123 Micro-managing arthropod invasions 2901 et al. 2002; Burnett et al. 2006). The movement of Adelges tsugae Annand (McClure 1990), while many biological invaders, and in particular arthro- long-range movement of the soybean , Aphis pods, often proceeds through a combination of local glycines Matsumura, is thought to be facilitated by population growth and short-range dispersal (i.e., atmospheric transport mechanisms (Venette and Fisher 1937; Skellam 1951; Okubo 1980) coupled Ragsdale 2004). Regardless of the mechanism of with long-range dispersal, in a process known as stratified dispersal, its existence has a fundamental stratified dispersal (Hengeveld 1989; Andow et al. effect on spread. Long-range dispersal events can 1990; Shigesada et al. 1995; Shigesada and Kawasaki initiate satellite colonies ahead of the distributional 1997) (Fig. 2). Although regulating short-range range in a process essentially analogous to the arrival movement is extremely challenging, managing satel- stage of biological invasions. If these colonies lite populations that arise outside of the established successfully establish, then they could grow and range through long-range dispersal can be a more eventually coalesce with the established range of the feasible goal with important consequences in limiting organism, resulting in a more rapid overall rate of overall range expansion (Liebhold and Tobin 2008). spread than what would be expected under exclu- In many non-native arthropods, the anthropogenic sively diffusive spread (Hengeveld 1989; Shigesada movement of life stages can be a dominant mode of and Kawasaki 1997; Liebhold and Tobin 2008). long-range displacement, though not an exclusive one Effective containment strategies rely on the early (National Research Council 2002). For example, detection of newly-established satellite colonies, and migratory birds are believed to facilitate the long- site-specific control tactics to effectively eradicate the distance dispersal of hemlock woolly adelgid, colonies prior to their increase in abundance and

Fig. 2 Stratified dispersal is the combination of short- and long-range dispersal. Colonies that arrive ahead of the moving population front through long-distance dispersal can grow and eventually coalesce with the expanding front over time

123 2902 A. E. Hajek, P. C. Tobin distribution. Once the organism is abundant and life stages (Sharov and Liebhold 1998b; Tobin and distributed over a broader range, eradication mea- Blackburn 2008; Hajek and Tobin 2009). Under STS, sures have decreased chances of success. In this pheromone-baited traps are deployed along the sense, containment strategies rely on the principles of population front to detect newly-established colonies, eradication although complete extirpation of the which can then be targeted for eradication to limit invasive species is not the goal. their influence on the rate of spread (Sharov and Many arthropod invaders are particularly prob- Liebhold 1998a, b). Because most newly-established lematic in human population centers where the colonies are detected at low densities, the primary economic impacts tend to be considerable due to management tactic in STS is mating disruption the high costs associated with conducting programs in (Thorpe et al. 2006; Tobin and Blackburn 2007), this complex environment and with subsequent which is very effective in areas where the maximum habitat reclamation (Nowak et al. 2001; Lard et al. pheromone-baited trap catch is \ 30 male moths/ 2002; Sydnor et al. 2007). This is especially true for trap. However, mating disruption is not effective at those invasive arthropods that cause damage to urban higher densities, and to manage these higher density forests where the hazards of tree mortality pose a populations, both Btk (Reardon et al. 1994) and liability to local governments and private individuals. LdMNPV (Reardon et al. 1996) are used (Fig. 3). In In naturalized areas, management strategies often STS, Btk doses generally range from 59 to 94 BIU/ need to consider the effects of control measures on ha, using either one or two applications during the non-target species, and in urban areas these concerns period of early instar activity. Several factors are extend to human health. In both cases, site-specific considered when determining the appropriate dose and host-specific control tactics are often desired, and and number of Btk applications, but the primary microbial pesticides generally provide the degree of factors to consider are the presence of egg masses target host specificity that limits environmental (which represents a reproducing population since contamination and non-target mortality. only males are detected in pheromone-baited traps), the initial male moth density, and the distance of the The gypsy moth slow-the-spread program treatment block from the infested area. Higher density infestations or those in which reproducing An example of the use of microbial pesticides in a populations have been confirmed are generally containment program to limit range expansion is the targeted using a higher Btk dose and/or an multiple gypsy moth Slow-the-Spread program (STS) (Tobin applications, while infestations that are farther away and Blackburn 2007). The gypsy moth occupies from the infested area are often targeted with a lower approximately 1/3 of the susceptible habitat in North dose but with multiple applications (Tobin and America, and continues to spread along an invasion Blackburn 2007; Hajek and Tobin 2009). This is front at variable rates (Johnson et al. 2006; Tobin because infestations farther away from the infested et al. 2007a, b). In addition to short-range dispersal, area contribute proportionally more to the rate of new satellite colonies arise through various mecha- spread under stratified dispersal than those that are nisms, including human and atmospheric transport of closer.

75

) (A) (B) 2 3000

50 2000

25 1000 Area treated (km treated Area 0 0 1980 1985 1990 1995 2000 2005 1980 1985 1990 1995 2000 2005

Fig. 3 Area treated with Btk (a) and LdMNPV (b) in gypsy moth population suppression (grey bars) and containment by Slow-the- Spread (black bars) management programs in the United States, 1980–2007 123 Micro-managing arthropod invasions 2903

A lesser used tactic under STS is application of Pathogenic, parasitic and predatory natural ene- LdMNPV (Fig. 3b). Because LdMNPV already occurs mies have been used to control invasive arthropods in in North America and is extremely host specific, it can a manner that is more environmentally safe than safely be used in environmentally-sensitive habitats synthetic chemical pesticides. Two major strategies when there is concern for the non-target effects of have been used against invasive arthropods: classical broader-spectrum pesticides, including Btk (which can biological control and inundative augmentation. adversely affect many species of Lepidoptera), or the Classical biological control is the ‘‘intentional intro- insect growth regulator diflubenzuron (which can duction of a non-native biological control agent for adversely affect all arthropods). Both Btk and dif- permanent establishment and long-term pest control’’ lubenzuron are often considered as having fewer and augmentation is application of natural enemies non-target and environmental effects than synthetic for immediate or sustained control that is not chemical pesticides. permanent (Eilenberg et al. 2001). Many species of insect predators and parasitoids have been released for classical biological control of invasive species Suppression of established invasive arthropod (Hoddle 2004), including against the gypsy moth populations using pathogens and parasitic during the early twentieth century (Burgess 1929). nematodes Both classical and augmentative biological control strategies have also been successfully used with In areas where invasive species have become estab- microbes targeting a diversity of invasive arthropods lished and are causing problems, efforts turn to (Table 3). controlling pest populations. Some invasive arthro- pods impact production agriculture and are managed Classical biological control using standard practices that incorporate the concept of economic injury thresholds (Pedigo et al. 1986), The attribute of classical biological control that often with a goal of near 100% mortality of the pest makes this strategy excellent for native ecosystems population. This type of intensive management could is the long-term effect, often with no further control be thought of as localized eradication efforts, e.g., in needed after natural enemy introduction and estab- agricultural fields. However, many of the species that lishment. However, for natural enemies with limited are included when using the term invasive are pests methods for self dispersal, classical biological control of native ecosystems or less managed systems such as programs can require mass production of the natural planted forests or urban forests. For pests in these enemy so that it can be further distributed throughout systems, the management goal is generally to main- the affected area. Over the past few decades, this tain the pest population at the lowest feasible level same permanence has lead to criticism based on and to preserve, or in some cases, re-establish the natural enemies released in the past that were not native ecosystem. In these instances, to attempt to adequately host-specific but had become permanently achieve high levels of pest mortality is simply not established (Henneman and Memmot 2001; Simberloff possible without considerable disruption to native and Stiling 1996; Strong and Pemberton 2000; Louda ecosystems or plantings near human habitation. The et al. 2003). As of 2007, it appeared that numbers of extent to which the invasive population can be classical biological control introductions of patho- suppressed is based on available methods for detec- gens and parasitic nematodes against arthropods tion and control, impact of the invasive species, had decreased from highs between 1970 and 1989 efficacy of the control agent, and available funding (Hajek et al. 2007), potentially due to concerns about and cooperation. The terms suppression, ‘mainte- non-target effects from classical biological control nance control’ (Schardt 1997) and ‘maintenance introductions. However, pathogens and nematodes management’ (Simberloff 2009) have been used to released for classical biological control have never describe this management concept aimed at suppress- been cited as causing non-target effects to the ing invasive populations and mitigating outbreak environment (Hajek et al. 2007), and testing to populations. ensure environmental safety of classical biological

123 2904 A. E. Hajek, P. C. Tobin

Table 3 Examples of successful uses of pathogens and nematodes for classical biological control and augmentation against invasive arthropods Type of application Agent Host Location Citations

Classical biological control Virus: Neodiprion Neodiprion sertifer Canada, United Hajek et al. (2005) sertifer (Geoffrey), European pine States and nucleopolyhedrovirus sawfly Scotland (NeseNPV) Classical biological control: Virus: Gilpinia Gilpinia hercyniae (Hartig), Canada and Hajek et al. (2005) Purposeful and accidental hercyniae European spruce sawfly United States introductions nucleopolyhedrovirus (GhNPV) Classical biological control: Fungus: Entomophaga Lymantria dispar (L.) United States and Solter and Hajek Accidental introduction maimaiga Humber, Canada (2009), see text resulting in establishment Shimazu & Soper Classical biological control Virus: Oryctes Oryctes rhinoceros (L.) and Islands in the Hajek et al. (2005), rhinoceros virus Oryctes monoceros South Pacific Jackson (2009) (OrV) (Olivier), Rhinoceros and Indian beetles Oceans Classical biological control Fungus: Zoophthora Therioaphis maculata Australia Nielsen and Wraight radicans Brefeld (Buckton), Spotted alfalfa (2009) (Batko) aphid Classical biological control Fungus: Neozygites Mononychellus tanajoa Benin Delalibera (2009) tanajoae Delalibera, Bondar, Cassava green Hajek & Humber mite Classical biological control Nematode: Steinernema Scapteriscus spp., mole Florida Hajek et al. (2005), and augmentative control scapterisci Nguyen & crickets Frank (2009) Smart Classical biological control Nematode: Deladenus Sirex noctilio F. Australia, New Bedding (2009) and augmentative control (= Beddingia) Zealand, siricidicola Bedding Augmentative control Fungus: Beauveria Monochamus alternatus Japan Shimazu (2009) bassiana (Balsamo) Hope Vuillemin Augmentative control: Bacterium: Bacillus Lymantria dispar (L.) United States Tobin and Blackburn Containment and thuringiensis var. (2007), Gypsy Moth suppression kurstaki HD-1 Digest (2009) Augmentative control: Virus: Lymantria dispar Lymantria dispar (L.) United States Tobin and Blackburn Containment and nucleopolyhedrovirus (2007), Gypsy Moth suppression (LdMNPV) Digest (2009) control agents has increased (Hoddle 2004; Hajek very subjective and results after establishment were et al. 2007). not reported for many of these programs. However, A recent summary of 121 classical biological some examples of successful programs are presented control introductions of pathogens and nematodes for in Table 3. Here, we will describe an example of a control of arthropods worldwide found that 63.6% classical biological control program against the gypsy targeted invasive rather than native pests (Hajek et al. moth. 2007). The majority of introduced pathogens and nematodes became established, regardless of whether The fungal pathogen, Entomophaga maimaiga, the host was native (71.4%) or non-native (72.4%). for control of the gypsy moth Unfortunately, it is difficult to state whether success- ful establishment resulted in successful control for Entomophaga maimaiga is native to Japan, north- many programs. Evaluating overall control can be eastern China, and the Russian Far East (Nielsen 123 Micro-managing arthropod invasions 2905 et al. 2005), while the gypsy moth is native to Europe, studies also suggest that E. maimaiga was not temperate Asia and northern Africa (Hajek 2007). successfully introduced from the 1985–1986 intro- Gypsy moth was introduced to North America in ductions and thus is considered to have been an 1869 and became the target of classical biological accidental introduction from Japan some time since control programs beginning in 1905 (Hajek 2007). In 1971. Although this possibility might sound outland- 1910–1911, the pathogen E. maimaiga that infects ish, other pathogens and nematodes have been gypsy moth larvae (then referred to as the ‘gypsy introduced accidentally (Hajek et al. 2007). In fact, fungus’), originating from two cadavers bearing LdMNPV was originally accidentally introduced to spores that had been collected from an area near North America some time before 1907 (Hajek et al. Tokyo, was introduced to areas adjacent to Boston, 2005). Massachusetts. By 1912, a monograph reported that An important aspect of any agent used for classical establishment of this entomopathogen had not been biological control is its specificity (Henneman and successful (Speare and Colley 1912). In 1985 and Memmot 2001; Simberloff and Stiling 1996; Strong 1986, an isolate of E. maimaiga from the western and Pemberton 2000; Louda et al. 2003). Extensive coast of Honshu was released in southwestern New studies of forest Lepidoptera have demonstrated that York State and Shenandoah National Park, Virginia, E. maimaiga could only have an impact on other respectively. Once again, establishment was not species in the Family Lymantriidae. However, other considered successful based on field studies at release lymantriids were not commonly infected in the field, sites in 1987 and 1989–1991 (Hajek et al. 2005). at least in part because they do not occupy the specific Thus, E. maimaiga was not known to be present in sites where infection risk is highest (Hajek 2007). North America when, in 1989, during a very wet spring E. maimaiga caused epizootics in lower Additional uses of microbes for classical density gypsy moth populations throughout seven biological control northeastern states in the US. By 1992, the fungus had spread across the contiguous distribution of A diversity of microbes introduced against several gypsy moth in the northeastern US (Hajek 2007). invasive species have become established, and pro- From 1992–2009, in central New York State, vided long-term control (Table 3). For example, as E. maimaiga has continued to cause infection each early as the late 1930s, a nucleopolyhedrovirus year and gypsy moth populations have not increased (NPV) appeared in populations of the invasive (Hajek 1997; AEH unpublished data). In contrast, European spruce sawfly, Gilpinia hercyniae (Hartig), E. maimaiga is considered to be present in the Mid- in Canada. This virus, thought to have been acciden- Atlantic area but it has not controlled gypsy moth tally introduced with parasitoids, became a key factor populations during recent outbreaks (1999–2002 and regulating populations of this defoliator (Cunningham 2006–2008) in this region (Gypsy Moth Digest 2009). 1998). It was subsequently introduced to Newfoundland The cause of the spatial variability in the activity of and used against an isolated infestation in Ontario as E. maimaiga in different regions is presently being part of classical biological control programs (Hajek investigated. et al. 2005). Viruses have also been successfully A major question has been the source of the introduced against the invasive rhinoceros beetle E. maimaiga introduction that began causing epizo- (Oryctes rhinoceros (L.)), fungi have been introduced otics in 1989. Molecular studies suggest that the against the invasive spotted alfalfa aphid in Australia E. maimaiga strains now active in North America did and cassava green mite in Benin, and nematodes have not originate from the 1910–1911 introductions been introduced against Sirex noctilio F. in the (Nielsen et al. 2005). In agreement, models of Southern Hemisphere and Scapteriscus mole crickets E. maimaiga activity comparing the influence of in Florida (Hajek et al. 2005, 2007). These introduced weather during different years suggest that microbes have always been very host specific, they E. maimaiga would have been detected if it was persist in the release areas and generally are able to present in 1945 or 1971 and, since it was not respond to increasing host densities (i.e., cause detected, E. maimaiga was most probably introduced epizootics) without repeated releases. Appropriate some time after 1971 (Weseloh 1998). Molecular microbes with these characteristics for introduction 123 2906 A. E. Hajek, P. C. Tobin against A. glabripennis or A. planipennis have not yet synchronous which can further exacerbate the eco- been identified, although efforts have been made to logical and socioeconomic impacts of these high- search for effective natural enemies in the native density populations (Johnson et al. 2005). Since 1924, ranges of these beetles. over 360,000 km2 have been defoliated by gypsy moth in the United States (Tobin et al. 2009). Many Augmentation biological control states maintain cooperative suppression programs in collaboration with local governments, private resi- Augmentation biological control takes two forms: dents, and the USDA, to mitigate gypsy moth application with effects only due to the actual outbreaks, and both Btk and LdMNPV are used in microbes applied (i.e., inundative control) or with these programs (Gypsy Moth Digest 2009). effects often delayed because the pathogen repro- duces in the pest population so that infection builds Use of Btk and LdMNPV for suppression of gypsy through time after application (i.e., inoculative con- moth outbreaks in the United States trol). Inundative augmentation is generally the strat- egy used for applying microbes for suppression, Gypsy moth is established throughout 12 states and in although it is understood that the pathogen probably portions of 6 additional states in the northeastern, replicates in the host to some extent, yielding further midwestern, and mid-Atlantic US (Tobin et al. 2009). infections. For inundative control with pathogens, in The principal material used to suppress established general the amount of the microbe applied is the gypsy moth populations in the United States is Btk amount of inoculum estimated as being present in the and, to a lesser extent, LdMNPV (Fig. 3). Since its environment during an epizootic. first use in gypsy moth suppression programs in 1980, Numerous species of bacteria, fungi, viruses and approximately 29,000 km2 have been treated with nematodes attacking arthropods have been developed Btk (Gypsy Moth Digest 2009) (Fig. 3a). During the for pest control (e.g., Lacey and Kaya 2007; de Faria recent outbreak between 2005 and 2007, Btk was and Wraight 2007), some of which are listed in used to treat 2,428 km2 under gypsy moth suppres- Table 3. The ability to mass produce the agent sion programs conducted by states, with single or relatively simply and inexpensively, and its ability double aerial applications of 60–89 billion interna- to retain viability during storage are important tional units (BIUs)/ha (Solter and Hajek 2009). This attributes determining which microbes are developed material is so extensively used because Btk can be as biopesticides. Species that have been developed as extremely effective at preventing outbreaks. The biopesticides have proved to provide control of the safety of this widely used biopesticide has been the intended pest with nonexistent to limited non-target subject of thousands of publications (see Garczynski effects (O’Callaghan and Brownbridge 2009). and Siegel 2007). As with many invasive arthropods, including the LdMNPV is well known for its ability to cause gypsy moth, most negative impacts are often associ- epizootics in high density gypsy moth populations, ated with outbreak populations (Leuschner et al. playing a significant part in natural regulation of 1996; Johnson et al. 2006). Therefore, a common gypsy moth populations (Elkinton and Liebhold approach to mitigate outbreaking populations is their 1990; Solter and Hajek 2009). This virus is consid- direct suppression, preferably prior to their reaching ered a valuable option for suppression because it is outbreaking densities. During gypsy moth outbreaks, not known to infect any other species. Its safety and for example, larvae can severely defoliate trees and ability to suppress gypsy moth populations have cause heavy tree mortality, especially to diseased, resulted in 40 years of product development. At stressed, or coniferous host trees (Scho¨nherr 1988; present LdMNPV is registered with the United States Herrick and Gansner 1987). Also, gypsy moth can be Environmental Protection Agency under the name a nuisance in recreational or residential areas due to Gypchek, for control of gypsy moth. For suppression, large numbers of caterpillars, quantities of their frass, two applications of 4.9 9 1011 occlusion bodies/ha, and presence of larval setae that can be allergenic to 3 days apart or one application of 9.9 9 1011 occlu- some individuals (Tuthill et al. 1984). Moreover, sion bodies/ha are usually applied aerially (Solter and gypsy moth outbreaks tend to be spatially Hajek 2009). Since its first use in gypsy moth 123 Micro-managing arthropod invasions 2907 suppression programs in 1988, approximately 283 km2 for augmentative control than those encountered have been treated using Gypchek,anaverageof during the development of microbes for use against, 14 km2/year (Gypsy Moth Digest 2009)(Fig.3b). for example, folivores. For gypsy moth suppression programs, the most Because some Bt endotoxins are active against important safety issue due to Btk applications is the beetles, appropriate strains of this bacterium have potential for effects on non-target Lepidoptera. Non- been explored for use against A. glabripennis. target lepidopteran abundance and species richness Initially, strains that were investigated were not are often impacted the year that Btk is applied, but virulent (D’Amico et al. 2004). However, a ceram- many impacted species increase again within a few bycid-active toxin has now been identified (=cry3Aa) years (Solter and Hajek 2009). However, the use of (Chen et al. 2005), although methods for application chemical insecticides often has a broader non-target so that adults or larvae would eat this material have effect than Btk, which is why, with the exception of eluded researchers, who state that ‘‘…the most the insect growth regulator diflubenzuron (registered effective deployment may require expression of the as Dimilin), chemical insecticides were not cry toxin genes in transgenic trees’’ (Hajek and Bauer included as treatment options under the gypsy moth 2009). Entomopathogenic fungi have also been Final Environmental Impact Statement (USDA developed against A. glabripennis, using a method 1995). State and Federal suppression programs can that takes advantage of contamination of adults with only use treatment options specified in the Final infective spores during their normal periods of Environmental Impact Statement to manage gypsy wandering on trunks and branches (Hajek and Bauer moth, and these include Btk, LdMNPV, diflubenzu- 2009). Hypocrealean fungi are grown in non-woven ron, mass trapping, mating disruption, and sterile fiber bands that are placed around tree branches. This insect release (Tobin and Blackburn 2007). More- application methodology is planned for use with an over, New Jersey, for example, has a state ban against attractant but, at this time, requires an industrial the use of diflubenzuron due to its non-target effects partner. Several species of entomopathogenic nema- (New Jersey Administrative Code Title 7, Chapter 30, todes have been shown to be effective at killing Subchapter 2). Alternatively, a do-nothing strategy A. glabripennis larvae and Steinernema feltiae also that could result in outbreaking gypsy moth popula- showed attraction to beetles (Solter et al. 2001; Fallon tions and consequent massive defoliation would also et al. 2004), which would help in host location under negatively impact larvae of non-target Lepidoptera as tree bark; however, to date, it is thought that well as other wildlife (Thurber et al. 1994; Redman entomopathogenic nematodes would need to be and Scriber 2000). injected into Asian longhorned beetle larval galleries to be effective. For A. planipennis, Bt galleriae (SDS-502) and its Use of microbes for augmentative control cry8Da toxin kill adult beetles after being sprayed of recently introduced invasive species onto foliage that the adults eat (Hajek and Bauer 2009). Efforts must now include formulation, droplet Some of the more recently introduced, high profile size, and droplet density analyses that, if successful, arthropod pests in North America include A. glab- would lead to registration of this Bt strain for ripennis and A. planipennis. Efforts are still being A. planipennis management. Entomopathogenic fungi made to eradicate local populations, and in these have also been investigated for control of emerald ash efforts, only agents that act very quickly would be borer adults and larvae by spraying trunks and foliage appropriate for eradication. Various species of patho- at different times of the season with Beauveria gens are currently under investigation against both of bassiana GHA (Liu and Bauer 2008a, b). This these wood borers to determine their feasibility in mycoinsecticide is already mass-produced in North eradication and in providing environmentally sensi- America so availability would not be a major tive control strategies if eradication is not successful. impediment. Methods have also been developed for Because both of these pests live within the tree during evaluating persistence of this fungus on tree trunks their immature stages, very different obstacles are and in soil at bases of trees after application in the being encountered toward development of microbes field (Castrillo et al. 2008). 123 2908 A. E. Hajek, P. C. Tobin

Discussion has been the focus of research efforts for over 100 years, we thus have a robust knowledge base on Increasing numbers of invasive arthropods are being gypsy moth biology, ecology, and management using introduced and are becoming established worldwide. pathogens. This wealth of knowledge potentially Eradication and management can be difficult but we provides a valuable template for determining if and are learning that specific tactics can work in some how entomopathogens could be applied feasibly cases (Simberloff 2009). Historically, chemical insec- against other invasive arthropod species. Some recent ticides were the mainstay of arthropod eradication high profile invasive arthropods include wood boring efforts, from arsenic-based compounds such as Paris beetles, in part due to the use of solid wood green to DDT to carbaryl. However, many invading packaging materials in which immatures can be arthropods frequently need to be eradicated or surreptitiously transported though global trade. Uses managed in natural ecosystems or areas of human of microbes against gypsy moth, with caterpillars habitation where concerns over human health and living and feeding externally on leaves, are not environmental safety are paramount and use of directly applicable to A. glabripennis and A. plani- chemical insecticides is prohibited or undesireable. pennis, with larval stages feeding within wood and Arthropod pathogens have been used for eradica- adults feeding high in tree canopies. Therefore, new tion, and arthropod pathogens and parasitic nema- approaches are being investigated toward the use of todes have been used for containment and suppression pathogens and nematodes for management of inva- of several invasive arthropod species. Pathogens that sive wood-borers. As more arthropod species become are used are safe to humans and generally have introduced, there will be an increased need to limited to no non-target effects (O’Callaghan and determine eradication feasibility and management Brownbridge 2009). Aside from safety issues, the guidelines, and the use of host-specific pathogens pathogens and nematodes that are used depend on the could be considered as one approach to investigate biological attributes of the pathogen or nematode, among several in these efforts. the control tactic being used (e.g., eradication, containment, classical biological control or augmen- Acknowledgments We thank L. Blackburn for assistance with tative biological control) and availability of the figures, M. Grambor for assistance with the manuscript and T. Ebata for assistance with providing information. Thought- pathogen or nematode. provoking comments from two anonymous reviewers were also There are many examples of successful eradication much appreciated. programs against the gypsy moth, and the majority of eradication efforts conducted over the last several decades have relied on Btk. In addition, gypsy moth References containment uses Btk as an important agent, in addition to mating disruption, to eliminate isolated Allwood AJ, Vueti ET, Leblanc L, Bull R (2002) Eradication of introduced Bactrocera species (Diptera: Tephritidae) in colonies that form ahead of the moving population Nauru using male annihilation and protein bait application front. In areas of the northeastern, eastern and techniques. In: Veitch CR, Clout MN (eds) Turning the midwestern United States where gypsy moth is well tide: The eradication of invasive species. Occasional established, suppression programs use a combination Paper of the IUCN Survival Commission 27, pp 19–25 Andow DA, Kareiva PM, Levin SA, Okubo A (1990) Spread of of a virus and a bacterium to mitigate outbreaks, invading organisms. Landsc Ecol 4:177–188 which can also be regulated by E. maimaiga epizo- Anonymous (1992) The new world screwworm eradication otics. Of course, eradication and containment of programme: North Africa 1988–1992. Food and Agri- gypsy moth is primarily possible due to the effec- culture of the United Nations Aronson AI, Beckman W, Dunn P (1986) Bacillus thuringi- tiveness of a monitoring tool, pheromone-baited ensis and related insect pathogens. Microbiol Rev 50:1–24 traps, in detecting newly-established and low density Barinaga M (1990) Entomologists in the Medfly maelstrom. populations, which are more feasible to eradicate. Science 247:1168–1169 We generally have very limited information about Bedding RA (2009) Controlling the pine-killing woodwasp, Sirex noctilio, with nematodes. In: Hajek AE, Glare TR, most invasive species, rendering their management O’Callaghan M (eds) Use of microbes for control and – with or without the use of entomopathogens eradication of invasive arthropods. Springer, Dordrecht, – extremely challenging. Because the gypsy moth pp 213–235 123 Micro-managing arthropod invasions 2909

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