FORUM Combining Tactics to Exploit Allee Effects for Eradication of Alien Populations

1 2 3 DAVID MAXWELL SUCKLING, PATRICK C. TOBIN, DEBORAH G. MCCULLOUGH, 4 AND DANIEL A. HERMS

J. Econ. Entomol. 105(1): 1Ð13 (2012); DOI: http://dx.doi.org/10.1603/EC11293 ABSTRACT Invasive species increasingly threaten ecosystems, food production, and human welfare worldwide. Hundreds of eradication programs have targeted a wide range of nonnative insect species to mitigate the economic and ecological impacts of biological invasions. Many such programs used multiple tactics to achieve this goal, but interactions between tactics have received little formal consideration, speciÞcally as they interact with Allee dynamics. If a population can be driven below an Allee threshold, extinction becomes more probable because of factors such as the failure to Þnd mates, satiate natural enemies, or successfully exploit food resources, as well as demographic and environmental stochasticity. A key implication of an Allee threshold is that the population can be eradicated without the need and expense of killing the last individuals. Some combinations of control tactics could interact with Allee dynamics to increase the probability of successful eradication. Combinations of tactics can be considered to have synergistic (greater efÞciency in achieving ex- tinction from the combination), additive (no improvement over single tactics alone), or antagonistic (reduced efÞciency from the combination) effects on Allee dynamics. We highlight examples of combinations of tactics likely to act synergistically, additively, or antagonistically on pest populations. By exploiting the interacting effects of multiple tactics on Allee dynamics, the success and cost- effectiveness of eradication programs can be enhanced.

KEY WORDS Allee effect, biological invasion, density dependence, eradication, invasive species

There has been a steady accumulation of an increas- (Wiedemann) (Diptera: Tephritidae), Cochliomyia ingly wide range of plant-feeding in forests, hominivorax Coquerel (Diptera: Calliphorida), Adel- agro-ecosystems, and urban environments postborder ges tsugae Annand (Hemiptera: Adelgidae), and Ly- and beyond their native range (Levine and DÕAntonio mantria dispar (L.) (Lepidoptera: Lymantriidae) cost 2003, Brockerhoff et al. 2006, Hulme et al. 2008, property owners, local and national government agen- Aukema et al. 2010). Most species that arrive in a new cies, and private industries billions of dollars annually habitat fail to establish (Williamson and Fitter 1996, (Aukema et al. 2010, 2011; Holmes et al. 2010; Kovacs Ludsin and Wolfe 2001, Simberloff and Gibbons 2004, et al. 2011). The distribution of costs from incursions Lockwood et al. 2005) or have relatively minor effects is often contentious. in their expanded range (Mack et al. 2000, Aukema et Preventing the introduction of species has long al. 2010). A portion of alien species, however, become been recognized as the most effective means to reduce invasive with substantial economic and ecological im- impacts of invaders (Sakai et al. 2001, Hulme et al. pacts, often increasing the energy footprint of food 2008, Liebhold and Tobin 2008). Numerous interna- and Þber production systems because of an increased tional phytosanitary regulations and agreements, be- need for pest management, or irreversibly altering the ginning in the United States with the 1912 U.S. Plant invaded ecosystem and its biodiversity (Pimentel Pest Act, have been implemented to reduce risks of 2002, Gandhi and Herms 2010, Aukema et al. 2011). inadvertent transport of insects and other organisms High proÞle invaders such as Agrilus planipennis Fair- through the movement of infested materials (e.g., U.S. maire (Coleoptera: Buprestidae), Ceratitis capitata Code of Federal Regulations, Title 7, Chapter III, Part 301). Nevertheless, nonnative insects continue to be 1 Corresponding author: The New Zealand Institute for Plant and introduced and newly established species are de- Food Research Ltd., PB 4704, Christchurch, New Zealand (e-mail: tected postborder every year (Work et al. 2005, Brock- [email protected]). 2 Forest Service, U.S. Department of Agriculture, Northern Re- erhoff et al. 2006, Liebhold et al. 2006, McCullough et search Station, Morgantown, WV 26505. al. 2006). Given current and projected rates of global 3 Departments of Entomology and Forestry, Michigan State Uni- trade and travel, it is inevitable that unwanted, non- versity, 243 Natural Science Building, East Lansing, MI 48824. native insects will continue to be introduced, and 4 Department of Entomology, Ohio Agricultural Research and Development Center, The Ohio State University, 1680 Madison Ave., some will establish and ultimately become invasive Wooster, OH 44691. pests.

0022-0493/12/0001Ð0013$04.00/0 ᭧ 2012 Entomological Society of America 2JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 105, no. 1

Options available for eradication or, in the event of failure or lack of feasibility, long-term management of invasive insects, depend on biological attributes, hosts and projected impacts of the pest. When an alien species is detected but expected to have little impact, regulatory agencies typically elect to take no action. In New Zealand, for example, an average of one new organism is discovered postborder every week (Kriti- cos et al. 2005), but eradication programs are rare and mounted only when there is a high probability of expected economic and environmental cost. Deci- sions to initiate an eradication program are not un- dertaken lightly, given the signiÞcant expense and potential controversy that often accompany such ef- forts (Kean et al. 2012), particularly so for multi-year projects (Knipling 1979). Moreover, if a nonnative species appears to be established across a large geo- graphic area, eradication is unlikely to be practical (Brockerhoff et al. 2010). Similarly, erroneously de- claring success is embarrassing and costly, and under- mines future conÞdence. Although there are hundreds of cases of successful Fig. 1. Allee dynamics resulting from combining treat- eradication programs (Kean et al. 2012), there remains ment tactics (dashed arrows). (A) Representation of Allee considerable pessimism about the feasibility of erad- dynamics in which the change in population density (Ntϩ1/ N ) is plotted against the initial density (N ). Initial densities ication (Dahlsten and Garcia 1989, Myers et al. 2000). t t above an Allee threshold (solid square) will lead to a positive Some failed eradication attempts can be attributed to rate of population increase until governed by overcrowding biological, tactical, resource or political limitations dynamics (e.g., a carrying capacity). Initial densities below (Myers et al. 1998, Government Accountability OfÞce an Allee threshold will lead to a declining population density 2006). The outcomes of some efforts remain ambigu- and extinction. (B) Synergistically combining a density-in- ous for reasons ranging from political aversion to an dependent tactic to reduce population density with one that admission of defeat, the difÞculty determining when a increases an Allee threshold. (C) Combining two tactics that population is truly eradicated, as well as the poten- do not affect density but jointly increase the Allee threshold. tially embarrassing and costly consequences of erro- (D) Combining two tactics that do not alter the Allee thresh- neously declaring success (Dreistadt 1983, Dreistadt old but jointly decrease population density below an Allee threshold. (E) Antagonistic combination of tactics in which and Weber 1989). To circumvent some of these chal- one decreases density while another negates an Allee effect. lenges, previous studies have described probabilistic models used to estimate the conÞdence that an erad- ication program was successful given a continual lack can be integrated into the design and implementation of detection in monitoring efforts (Barclay and Har- of operational eradication programs (Tobin et al. grove 2005, Kean and Suckling 2005). Ultimately, the 2011). A key concept is that of pest density, which damage or potential damage associated with a non- involves knowledge of the number of individuals per native species must warrant the investment required unit area. Pest control tactics can be broadly classiÞed to detect and eradicate the population, and viable as density-independent, such as insecticide applica- methods to do so must be available. Given the long- tions where a certain proportion of the population is term costs of damage and pest management averted by killed, or density-dependent, such as mating disrup- eradication (Popham and Hall 1958, Klassen 1989, tion, where efÞcacy is inversely dependent on the Brockerhoff et al. 2010), eradication should not be absolute density and scarcity plays a role. Tactics discounted as an option, especially if novel approaches could also be used to subdivide or fragment popula- can facilitate success. Advances in understanding and tions, which can then be progressively tackled using technology can generate new tactics or strategies that the rolling carpet principle (Dyck et al. 2005). can be used in programs to eradicate insect pests. For In many populations, there is a critical population example, identiÞcation and synthesis of long-range size or density, known as the Allee threshold, below pheromones and other attractants have provided which the per capita population growth rate is nega- highly effective detection tools, and facilitated their tive and the population proceeds toward extinction use as species speciÞc and environmentally benign (Fig. 1A; Courchamp et al. 1999, 2008; Berec et al. control tactics (e.g., mating disruption or mass trap- 2007). Allee effects may arise from intrinsic biological ping) (Carde´ and Minks 1995, El-Sayed 2011). traits of the organism, or its interactions with its host, Our understanding of the population ecology of natural enemies or other aspects of its environment. invasive species (Sakai et al. 2001) and in particular, Individuals within a sexually reproducing population, the role of Allee dynamics in biological invasions for example, are less likely to locate a suitable mate at (Taylor and Hastings 2005, Liebhold and Tobin 2008), low than at high densities (Tobin et al. 2009, Rhainds has increased in recent years, generating concepts that 2010). Some insects, such as mass-attacking bark bee- February 2012 SUCKLING ET AL.: INSECT ERADICATION 3 tles, rely on high densities to overcome tree defenses selection and integration of tactics, and the likelihood and successfully colonize hosts (Raffa and Berryman of success. In this review, we identify and summarize 1983, Boone et al. 2011), a strategy that is less effective individual tactics that have been or could be used in sparse populations. Moreover, demographic sto- effectively against target pests, and highlight the rel- chasticity alone has been shown to induce an Allee- evance of Allee dynamics to eradication programs. like effect, which also can challenge the viability of Where speciÞc case studies related to eradication are low-density populations (Lande 1998). Allee effects, limited, we have drawn on relevant examples of tactics therefore, function as density-dependent factors af- used in integrated pest management (IPM) programs, fecting population dynamics through altering the rate which may also be potentially suitable for use in erad- of population increase (Dennis 1989, Stephens et al. ication programs. We then consider the integration of 1999). The application of tactics that reduce the like- two tactics (for simplicity) within the context of Allee lihood of mate Þnding, consequently resulting in a dynamics, and how combinations of tactics can affect reduced population growth rate, is an example be- the prospect of successful eradication. cause population density would be reduced over time. Consequences of Allee effects are reßected in unsuc- Single Tactics cessful classical biological control attempts; successful establishment of natural enemies most often occurred Delimitation Technologies. The ability to efÞ- when relatively high densities of organisms are re- ciently detect and delineate incipient, low-density leased (Beirne 1975, Stiling 1990, Hopper and Roush populations of unwanted organisms is often a key 1993, Fagan et al. 2002). aspect of successful eradication programs (Rejma´nek An under-appreciated implication of Allee dynam- and Pitcairn 2002, Brockerhoff et al. 2010). Traps ics is that not every individual must be killed to erad- baited with attractants such as pheromones or host icate a pest population (Liebhold and Bascompte plant volatiles are frequently used in eradication pro- 2003, Liebhold and Tobin 2008), a concept originally grams, as well as pest management efforts (El-Sayed derived from conservation programs designed to pre- 2011). Examples include the use of pheromone-baited vent the extirpation of endangered species (Lande traps to detect populations of lepidopteran species 1988, Courchamp and Macdonald 2001, Courchamp et including European and Asian strains of L. dispar in al. 2008). For those species inßuenced by Allee effects, North America (Tobin and Blackburn 2007), and Or- a minimum number of individuals is required for a gyia thyellina Butler (Lepidoptera: Lymantriidae) population to remain viable. If an eradication program (Hosking 2003) and Hyphantria cunea (Drury) (Lep- can drive the pest population below the Allee thresh- idoptera: Arctiidae) in New Zealand (El-Sayed et al. old, eradication can be achieved without the relatively 2005). Traps baited with pheromone or host plant costly efforts to locate and kill the last remaining volatiles have also been widely used to detect or mon- individuals. Although newly established populations, itor scolytinid bark and ambrosia (Moeck 1970; when detected at low density, tend to be the most Borden 1989, 1997). Trap logs or trees that produce amenable to eradication, it is also important to con- attractive volatiles have proved useful in combination sider the interaction between density and the spatial with or in the absence of pheromones (Samways 1987; extent of the population, which could vary between Bakke 1989; McCullough et al. 2009a, b; Smith et al. life stages and over time (Vercken et al. 2011). Re- 2009). gardless, when a local population is suppressed below Insecticides. Insecticides can be delivered to an the Allee threshold, extinction becomes increasingly unwanted insect population through a variety of probable. Thus, while Allee effects are the bane of mechanisms, including aerial or ground sprays, trunk conservation biologists (Courchamp et al. 2008), they injections or soil applications of systemic products, can be a beneÞt in nonnative species management and lure and kill technologies. Historically, broad- (Tobin et al. 2011). Species subject to strong Allee spectrum insecticide sprays were widely used in insect effects are likely to be more amenable to eradication eradications (Herms and McCullough 2011), but are than species not governed by Allee dynamics or by rare today given concerns about drift, environmental only weak Allee effects (Liebhold and Tobin 2008). contamination, exposure, and nontarget effects. Moreover, Allee effects can affect the rate of spread of Advances in insecticide formulation and delivery invading organisms (Lewis and Kareiva 1993, Taylor et systems can mitigate some risks, and relatively new al. 2004, Johnson et al. 2006, Tobin et al. 2007). Pro- products may be more acceptable for eradication pro- grams designed to reduce spread rates are thus more grams or invasive pest management efforts than sprays likely to be successful against species subject to Allee of broad spectrum insecticides. Localized applications dynamics (Sharov and Liebhold 1998, Liebhold et al. of insecticide products containing neonicotinoids, 2007). While Allee effects may reduce the Þnal treat- avermectin, or azadirachtin applied to ornamental ment costs in eradication, posttreatment surveillance trees via trunk or stem injections, for example, sub- costs will usually be incurred to demonstrate that stantially reduce undesirable effects associated with eradication has been achieved. cover sprays (Herms et al. 2009). While selective in- Coupling population theory with a mechanistic un- secticides and biopesticides are generally preferred derstanding of diverse intervention technologies can for operational programs (Hajek and Tobin 2010), improve the quality of decisions related to the erad- they may be more expensive. Repeated applications ication of nonnative insect species, the cost effective may be needed to offset relatively short persistence of 4JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 105, no. 1 some products, such as Bacillus thuringiensis Berliner naturally occurring hemlocks in the vicinity of the (Bacillales: Bacillaceae) (Garczynski and Siegel infested plantings were either destroyed or treated 2007). The kurstaki strain of B. thuringiensis continues with systemic insecticides over a 3-yr period (Kean et to be widely used against L. dispar in both eradication al. 2012). These successful eradication projects af- and barrier zone management programs in North fected relatively few landowners and nursery owners, America (Hajek and Tobin 2010), and was used to who were generally cooperative with regulatory ofÞ- successfully eradicate O. thyellina (Hosking 2003) and cials (D.A.H. and D.G.M., unpublished data). Teia anartoides (Lepidoptera: Lymantriidae) from Large-scale projects that encompass host tree de- Auckland, New Zealand (Suckling et al. 2007). Al- struction, however, frequently engender controversy, though public opposition to the aerial application of B. and logistical arrangements can be costly and com- thuringiensis over urban areas can be considerable plex, although they have frequently formed a major (Hosking 2003, Hajek and Tobin 2010), the long-term, tactic during eradication programs (Kean et al. 2012). nontarget impacts of this tactic are generally low There has often been a role for compensation pay- (Sample et al. 1996, Glare and OÕCallaghan 2000, ments (cash or in kind) in host destruction schemes, Herms 2003, Gandhi and Herms 2010). In contrast, that is important for acceptance in some cases. De- aerial applications of the growth regulator dißuben- struction of infested spruce trees in a Nova Scotia park zuron have been shown to have broad-spectrum, per- for Tetropium fuscum (F.) (Coleoptera: Cerambyci- sistent impacts on nontarget organisms that can cas- dae) eradication sparked considerable public protest cade across trophic levels (Martinat et al. 1988, Eisler for the loss of amenity value (Henry et al. 2005). Ash 1992, Butler et al. 1997). Other IGRs, juvenile hor- tree destruction, designed to ensure infested but mone analogues, ecdysone agonists, and macrocyclic asymptomatic trees were eliminated, was used in sev- lactones (such as the spinosyns) are somewhat selec- eral projects designed to eradicate localized infesta- tive. tions of A. planipennis beginning in 2003 (Herms and Some entomopathogen products such as the L. dis- McCullough 2011). Although most ash trees in any par nucleopolyhedrosis virus, commercially regis- given project area were relatively small (McCullough tered as Gypchek (Reardon et al. 1996), can be pro- and Siegert 2007, Siegert et al. 2010), thousands of duced economically, and applied over large areas. trees were removed from forests, riverbanks, residen- EfÞcacy of entomopathogen products varies consid- tial and urban areas (Cappaert et al. 2005, Stone et al. erably and could be inßuenced by temperature, mois- 2005, Poland and McCullough 2006). Efforts to erad- ture, or other environmental conditions (Ignoffo icate Anoplophora glabripennis Motschulsky (Co- 1992). Many are highly speciÞc and present little risk leoptera: Cerambycidae) in the United States and to nontarget organisms (Hajek and Tobin 2010), while Canada have similarly required destruction of infested others, such as the fungal pathogen Beauveria bassi- or potentially infested host trees (Smith et al. 2009). ana, can affect a relatively broad range of insects Most of these programs were centered in urban and (Goettel et al. 1990). Use of some entomopathogen residential areas, and sometimes eliminated a substan- products can also be limited by the need for in vivo tial portion of the canopy. Public perception and ac- production, which requires mass rearing facilities to ceptance of the host destruction components in the A. produce sufÞcient quantities for application (Reardon planipennis and A. glabripennis programs have ranged et al. 1996). In addition, there are few examples of from supportive to vehement opposition (Smith et al. entomopathogens that effectively control phloem- or 2009). wood-boring insects. Semiochemical Approaches. One semiochemical Host Destruction. Removal of host plants can be approach used for numerous lepidopteran pests is used as a means to reduce populations and limit spread mating disruption, in which large quantities of female of nonnative pests (Hardee and Harris 2003, Cappaert moth synthetic sex pheromone are released to disrupt et al. 2005, Smith et al. 2009). Success of such efforts the ability of males to locate calling females (Carde´ can depend on the scale, location, economic sector and Minks 1995, Witzgall et al. 2010). Continual ex- affected, and the ability of regulatory ofÞcials to en- posure to high levels of pheromones may shut down force compliance. Early efforts to contain or eradicate male searching behavior because of habituation, or L. dispar populations in the northeastern United males may be simply unable to locate mates, resulting States, for example, included felling and burning in- in decreased populations or local extirpation (Ya- fested sections of forests (Herms and McCullough manaka 2007). This tactic, which has negligible effects 2011). Destruction of thousands of apple trees across on nontarget organisms or the environment, has been 790 km2 in Brazil beginning in the late 1990s was effectively used in L. dispar eradication programs credited with substantially reducing populations of C. (Dreistadt and Weber 1989, USDA Forest Service pomonella. This effort received major support from 2010), and is also the preferred control tactic in L. apple growers and the Ministry of Agriculture, with dispar barrier zone management (Tobin and Black- both groups allocating personnel, funds, and equip- burn 2007). Mating disruption has also been evaluated ment to the campaign (Kovaleski and Mumford 2007). for indigenous lepidopteran defoliators including Cho- In Michigan and Ohio, localized populations of A. ristoneura fumiferana (Clemens) (Lepidoptera: Tor- tsugae became established when infested nursery tricidae), Dasychira plagiata (Walker) (Lepidoptera: trees were planted in residential areas, and trees Lymantriidae), and Orgyia pseudotsugata (McDun- known to be infested were destroyed. Planted and nough) (Lepidoptera: Lymantriidae) (El-Sayed February 2012 SUCKLING ET AL.: INSECT ERADICATION 5

2011), and wood-borers including Synanthedon spp. ment (Vreysen et al. 2007). Sterility results from the (Lepidoptera: Sesiidae) (PÞeffer et al. 1991, Matsu- induction of dominant lethal mutations in irradiated moto et al. 2007, Leskey et al. 2009). This technology sperm or eggs. In operational programs, sterilized in- may have utility in eradication programs should these sects are released en masse, with the goal of reducing pests become established outside their native range. production of viable eggs by the pest. This tactic, Other semiochemical-based approaches to pest however, is density dependent because it is more management include mass trapping (Schlyter et al. effective in low-density populations than higher den- 2003, El-Sayed et al. 2006) and lure and kill (Foster and sity ones (Knipling et al. 1979) and is therefore most Harris 1997, El-Sayed et al. 2009). Both tactics involve effective at the start or end of a response when the the attraction and subsequent removal of individuals target population is small. Other potential barriers from the population. This approach has been used for include the ability of sterilized insects to outcompete suppression of native (Silverstein 1981, Borden 1989) wild insects for mates, the need to mass rear viable and nonnative bark beetles (McCullough and Sadof individuals, and the capability to transport sterilized 1998), and in eradication efforts against L. dispar insects of high Þtness from rearing facilities to the (USDA Forest Service 2010) and Anthonomous gran- target population. dis Boheman (Coleoptera: Curcurlionidae) (El-Sayed SIT played a major role in the successful eradication et al. 2006). Unfortunately, while phloem- and wood- of Cochliomyia hominivorax (Coquerel) (Diptera: boring beetles comprise a substantial and increasingly Calliphoridae) in the United States, Mexico, and Latin large proportion of new invaders (Aukema et al. 2010), America (Wyss 2000), and has been used against te- many do not use long range pheromones (Hardie and phritid fruit ßies in numerous locations (Hendrichs Minks 1999), including prominent invaders such as 2002, Klassen and Curtis 2005). This tactic was also Agrilus planipennis and Anoplophora glabripennis used against (Fairmaire) (Co- (Cappaert et al. 2005, Smith et al. 2009). Moreover, leoptera: ) in Japan (Moriya and Mi- while mass trapping has the potential to eradicate or yatake 2001). Two large, area-wide SIT programs were suppress low-density, isolated pest populations (El- used successfully to eradicate Pectinophora gossypiella Sayed et al. 2006, Yamanaka 2007), it can be logistically (Saunders) (Lepidoptera: Gelechiidae) in California challenging to use effectively because of low trap and Cydia pomonella L. (Lepidoptera: Tortricidae) in efÞciency, trap saturation, the lack of trap selectivity, British Columbia (Bloem et al. 2007). Smaller pro- and the need for high trap density and hence high cost. grams targeting other Lepidoptera have also been un- In some cases, pheromones used as kairomones by dertaken (Suckling et al. 2007, Vreysen et al. 2007). predators or parasitoids of the target pest have the Public opposition to aerial insecticide applications to potential to interfere with biological control if large eradicate C. capitata outbreaks in California and Flor- numbers of natural enemies are also trapped (Herms ida led to the year-round, prophylactic release of ster- et al. 1991, Dahlsten et al. 2004). ile ßies in these areas beginning in 1994 (Enkerlin Semiochemical-based tactics can also be used to 2005). Recent interviews with stakeholders in New disrupt pheromone-based, mass attack behavior of Zealand asked for their preference among three treat- certain bark species that would normally facil- ments tactics used in eradication; the greatest prefer- itate successful colonization of live host trees (Borden ence was for the sterile insect technique followed by 1989, 1997; Raffa 2001, Boone et al. 2011). For example, aerial applications of pheromone and lastly aerial ap- at least 40 attacks per square meter of bark surface plications of B. thuringiensis (Gamble et al. 2010). were required for Dendroctonus ponderosae Hopkins Biological Control. Classical biological control, the (Coleoptera: Curcurlionidae) to overcome tree de- deliberate introduction of nonnative natural enemies fenses (Raffa and Berryman 1983). The inability of of a pest, is rarely compatible with the goal of eradi- low-density, founder populations to successfully mass cation, in part because approval for release of new attack hosts in a new environment may explain why Ips agents generally involves relatively long time frames. typographus (L.) (Coleoptera: Curculionidae) has This process can be especially protracted when for- failed to establish outside its native range (Gre´goire et eign exploration, importation, and host speciÞcity al. 2006), despite frequent introductions (Brockerhoff studies to avoid detrimental effects to nontarget spe- et al. 2006). Potential also exists for semiochemicals to cies are required. However, where it is possible to be used in push-pull strategies (Cook et al. 2007), predict threats from rapid geographic expansion and where disruptants or repellant compounds ÔpushÕ bee- risk assessment, initiating steps to identify and evalu- tles away from susceptible hosts and ÔpullÕ them to- ate natural enemies for potential biocontrol efforts ward baited traps or trap trees. Such an approach may be prudent as it may be possible to gain prior successfully protected a rare stand of Torrey Pines approval, especially where the biological control from Ips paraconfusus bark beetles in California (Shea agent has been efÞcacious in previously invaded areas. and Neustein 1995) and was used effectively in some Natural enemies can presumably mediate Allee ef- stands to deter attack by D. ponderosae (Borden et al. fects in populations of their prey (Gascoigne and Lip- 2006). cius 2004, Gregory and Courchamp 2010, McLellan et Sterile Insect Technique. The sterile insect tech- al. 2010), which could have application in eradication nique (SIT) (Knipling 1959, 1979) has been used in programs, but empirical examples are rare. Introduc- several insect eradication programs and has no ad- tion of the generalist parasitoid Compsilura concinnata verse effects on nontarget organisms or the environ- (Meigen) (Diptera: Tachinidae) into North America 6JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 105, no. 1

Table 1. Potential outcomes when combining tactics (A and B) hypothesized to be density-dependent (DD) or density-independent (DI) in insect eradication compared with single tactics alone

Combination Quality of Examples type interaction Synergistic AB Ͼ A ϩ B 1. Inundative biocontrol (DD) ϩ SIT (DD) 2. Mating disruption (DD) ϩ SIT (DD) 3. Transgenic host plants (DI) ϩ SIT (DD) 4. Insecticides (DI) ϩ mass trapping (DD) 5. Insecticides (DI) ϩ mating disruption (DD) 6. Mating disruption (DD) ϩ lure and kill (DD) (when using different semiochemicals) Additive AB ϭ A ϩ B 1. Insecticides (DI) ϩ host destruction (DI) 2. Selective insecticides (DI) ϩ innundative biocontrol (DI) 3. Two insecticides targeting different life stages (DI) Redundant AB ϭ A or B 1. Broad-spectrum insecticide (DI) ϩ innundative biocontrol (DD) 2. Broad-spectrum insecticide (DI) followed by selective insecticide (DI) 3. Mating disruption (DD) ϩ lure and kill (DD) (same semiochemical) Antagonistic AB Ͻ A ϩ B 1. SIT (DD) and mass trapping (DD) (trap saturation) 2. Broad-spectrum insecticides (DI) ϩ biocontrol (DD) (pest resurgence through natural enemy mortality) for L. dispar control has been credited with causing control tactics can be combined to exploit different local extinctions and dramatically reducing remaining causes of an Allee effect or to act synergistically on one populations of the invasive Euproctis chrysorrhoea (L.) cause of an Allee effect. Indeed, recent work has (Lepidoptera: Lymantriidae) in areas of the north- suggested that multiple causes of an Allee effect are eastern United States (Elkinton et al. 2006). Unfortu- not necessarily additive, but instead may interact in a nately, this parasitoid also attacks many nontarget complex way (Berec et al. 2007). Thus, identifying the Lepidoptera species in North America (Parry 2009), most efÞcient combinations of tactics to use against and may be responsible for major declines in native populations subject to Allee dynamics can facilitate saturniid populations (Boettner et al. 2000). Release of successful eradication. Regardless of the tactics used, the parasitoid Bessa remota (Aldrich) (Diptera: Ta- both the efÞciency and potential success of eradica- chinidae) is believed to have caused the extirpation of tion can be enhanced by considering the interactions its target host, Levuana iridescens Betheune-Baker between or among tactics. We consider the following (Lepidoptera: Zygaenidae), in Fiji (Hoddle 2006). categories of tactic interactions: synergistic, additive, Inundative release of native or previously established redundant, and antagonistic (Table 1; Fig. 1). parasitoids or predators could also presumably act to Synergystic Interaction. Combining two (or more) suppress or limit spread of a localized pest population. tactics to generate a synergistic interaction is ideal, The use of natural enemies for biocontrol, however, is regardless of whether Allee dynamics are exploited more often a strategy for long-term management of (Fig. 1BÐC) or not (Fig. 1D) (Barclay and Li 1991). nonnative species and restoration of ecosystems de- Several options for combining treatment tactics to graded by invasive species (Hoddle 2004). Although speciÞcally enhance or exploit an Allee effect are such releases have rarely played a role in eradication listed in Table 1. Synergistic effects could be achieved efforts, biological control could potentially act syner- by combining a density-independent tactic that re- gistically in combination with other tactics such as egg duces pest density with a density-dependent tactic parasitism with releases of sterile females (Cossentine and Jensen 2000, Carpenter et al. 2004). that increases the Allee threshold (Fig. 1B; Berec et al. 2007). This interaction is particularly relevant for eradication because it can enhance program effec- Multiple Tactic Combinations tiveness by increasing the beneÞt-to-cost ratio. For When developing an eradication strategy for an example, mating disruption with pheromone applica- insect pest, it could be tempting to simply deploy all tion can be an effective, density-dependent tactic at available tactics as rapidly as possible within Þnancial low population densities, but is generally ineffective at constraints. Indeed, a primary challenge in eradication higher densities because of visual mate location (Ro- is the availability of sufÞcient funds to achieve success elofs et al. 1970, Carde´ and Minks 1995, Sharov et al. (Brockerhoff et al. 2010, Kean et al. 2012). Potential 2002, Yamanaka 2007). Insecticide applications or host interactions between tactics used either simultane- removal are both density-independent tactics that can ously or sequentially can be positive or negative be used at higher pest densities, but removing a suf- (Knipling 1979, Barclay 1992) and warrant consider- Þcient number of individuals to drive a population ation when an eradication strategy is developed. Un- below an Allee threshold may not be cost-effective or derstanding and incorporating Allee effects (Fig. 1A; practical. Decreasing pest density with insecticides Allee 1938, Stephens et al. 1999) into operational pro- followed by pheromone applications to disrupt mating grams can strongly inßuence costs and success of erad- of surviving adults can act synergistically by reducing ication efforts. Because there could be many causes of the overall population density and concurrently in- an Allee effect (Courchamp et al. 2008), multiple creasing the Allee threshold (Fig. 1B). February 2012 SUCKLING ET AL.: INSECT ERADICATION 7

Other desirable combinations include two density- used, it is important to highlight them in our efforts to dependent tactics that jointly increase the Allee illustrate the utility of synergistic interactions. threshold without affecting population density (Fig. Antagonostic Interaction. Regardless of the tactics 1C), or two density-independent tactics that do not used, multiple tactics should not, in principle, interact alter the Allee threshold but jointly decrease the pop- in an antagonistic manner (Table 1; Fig. 1E). Combi- ulation density below an Allee threshold (Fig. 1D). nations of tactics can have antagonistic consequences, Examples of successful combination of tactics include which clearly would be counterproductive to eradi- inundative release of Trichogramma egg parasitoids cation efforts. For example, if an insecticide applica- followed by SIT, which acted synergistically to reduce tion killed predatory insects that would otherwise populations of C. pomonella (Bleom et al. 1998, Cos- prey upon any residual pest population, the combi- sentine and Jensen 2000). Carpenter et al. (2004) nation could be considered antagonistic and poten- determined that the combined effect of using both tially negate the effect of a predator-driven Allee ef- tactics exceeded the effects of deploying each tactic in fect (Fig. 1E; Gascoigne and Lipcius 2004, Gregory isolation because the sterile eggs laid by irradiated and Courchamp 2010, McLellan et al. 2010). A simul- moths enhanced the parasitoid population. A combi- taneous combination of SIT and mass trapping could nation of mating disruption and SIT, two density- also be counterproductive. Sterile insects would be dependent tactics, could also be synergistic (Bloem et removed from the population while the efÞcacy of al. 2007); while no individuals are killed directly, the mass trapping would be reduced if traps were satu- increased Allee threshold may lead to a decline in the rated by large numbers of sterile insects. Pest sup- pest population (Fig. 1C). An area-wide eradication pression tactics can also interfere with surveillance program against the cotton pest P. gossypiella incor- programs to detect, delimit, or monitor the pest pop- porated mating disruption, insecticides and SIT, a ulation. Pheromone-baited traps, for example, can be combination that acted synergistically with transgenic silenced by widespread application of pheromone ap- cotton (containing B. thuringiensis) (Simmons et al. plied for mating disruption (Thorpe et al. 2007), a 2007). Releasing parasitoids to attack larval stages of critical concern when trap catch data are needed for the pest combined with SIT, which acts on the adults decision-making (Tobin and Blackburn 2007). While could also be synergistic (Barclay and Li 1991). Ad- it is also possible that these traps are not silenced through mating disruption but rather indicate treat- ditional potentially synergistic combinations can be ment efÞcacy, poorly conceived combinations are still postulated, such as release of a sex pheromone to counterproductive and the possible interactions need disrupt mating or achieve mass trapping, coupled with to be examined carefully. In the case where mass a female attractant-based lure and kill system. At pres- baiting to detect fruit ßies also masks the presence of ent, most mass trapping systems target males. traps to an extent, it could be worthwhile to deploy Additive Interaction. An additive interaction in- traps because they can still provide relatively cheap volves two treatment tactics that act neither syner- information compared with rearing from randomly gistically or antagonistically. Two density indepen- sampled host fruits. dent tactics, such as two insecticides that each target In many cases, efÞcacy of different tactics varies a different life stage, likely act in an additive manner with pest density and combining tactics requires because each reduces the population density inde- consideration of the spatial distribution of the in- pendently of each other. Although this is a suitable vasive pest population. In particular, tactics that are combination of tactics for eradication because the density-independent could be used broadly across a continuous reduction of population density could still pestÕs spatial distribution, while density-dependent render a population below an Allee threshold (Fig. tactics may be effective only in speciÞc areas. To 1D), it requires more effort than synergistic combi- further optimize an eradication strategy, culling, nations of tactics. Depending upon the circumstance, host removal, and other density-independent tactics tactics that generally interact in an additive manner could be used initially against high density popula- could interact synergistically; for example, application tions within the infested area, followed by imple- of a selective insecticide application could be syner- mentation of density-dependent tactics, such as gistic with biological control if the biological control mating disruption (Fig. 2). agent displayed nonrandom searching behavior and However, insecticide application combined with speciÞcally sought out residual members of the pop- biocontrol could function in an additive or possibly ulation that were not targeted by the insecticide (Bar- synergist manner if, for example, a parasitoid displayed clay 1987, Barclay and Chao 1991). nonrandom searching behavior (Barclay 1987, Barclay Redundant Interaction. To be cost-effective, it is and Li 1991). Regardless of the tactics used, both the also important to avoid combining tactics that are efÞciency and potential success of eradication can be redundant, where tactics overlap in effect, or super- enhanced by considering the interactions between or sede each other (Table 1). Examples include the con- among tactics. current use of a broad-spectrum and a selective in- We conclude that despite the importance of erad- secticide, two density-independent tactics, or the ication as a management tool for averting the long- concurrent use of mating disruption and lure-and-kill, term economic, social and environmental costs of in- two density-dependent tactics. Although in practice vasive species, fundamental theoretical underpinnings these types of tactic combinations are rarely, if ever, of eradication strategies are not well-developed. The 8JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 105, no. 1

Fig. 2. Combining treatment tactics in space and time. A spatial representation of an insect population, from low (blue) to high (red)densities at time t. High density areas are treated at time t using a density-independent tactic, such as a pesticide, resulting in a decrease in density. At time t ϩ 1, the remaining population is managed using a density-dependent tactic, such as mating disruption, to increase the Allee threshold. At time t ϩ 2, the remaining population density is below the Allee threshold, and the population declines toward extinction. number of eradication programs has risen steadily as will facilitate efforts to suppress or eradicate pest pop- globalization has increased, and hundreds of insect ulations, particularly if synergistic interactions can be eradication programs have now been documented achieved and exploited. Ideally, the likely effect of (Kean et al. 2012). Critics of insect eradication have potential tactics used alone and in combinations suggested that such programs seldom succeed (e.g., should be considered early in the development of an Myers et al. 2000), perhaps because of a number of eradication strategy and potentially synergistic com- high-proÞle eradication failures. There is evidence, binations should be used when and where possible. however, that many eradication efforts have indeed We have highlighted how eradication tactics can be been successful, most often at a state or regional rather combined in strategic and sometimes counter-intui- than continental scales (Kean et al. 2012), although tive ways to simultaneously manipulate pest density there are prominent examples of successful wide-scale and Allee dynamics to achieve eradication. We rec- eradiction programs (Klassen 1989, Wyss 2000, ognize, however, that eradication of some insect Hardee and Harris 2003). It seems clear that insect groups is currently more feasible than others. Many eradication is more feasible and cost-effective than has lepidopteran defoliators, for example, respond to long- been generally recognized (Brockerhoff et al. 2010, range sex pheromones and remain exposed for much Kean et al. 2012). of their life cycle to natural enemies, microbial insec- Advances in population biology have practical im- ticides or entomopathogens. Unfortunately, there are plications for eradication programs in the same way clear knowledge gaps and limited means to effectively that they inßuence programs designed to conserve detect, trap or control other groups including sap- and protect rare species from extinction (Courchamp feeders and many phloem- and wood-boring species. et al. 2008). While the goals are different, the same New strategies and technology to identify and exploit principles constrain low-density populations of an in- Allee thresholds and synergistic combinations of con- vasive pest or an endangered species. Understanding trol tactics are especially needed to deal with these and exploiting Allee effects that may facilitate eradi- invaders, which comprise a substantial portion of the cation is especially important because resources need damaging invasive pests in North America (Langor et not be expended to locate and kill every individual of al. 2009, Aukema et al. 2010). BeneÞts associated with the target pest (Liebhold and Tobin 2008). Once pop- implementing control tactics alone or in combinations ulations are suppressed below the Allee threshold, will need to be evaluated to justify program costs extinction is likely to occur without further interven- (Barclay and Li 1991), but the prospect of increasing tion. Understanding interactions when tactics are the success of eradication programs is a strong incen- combined (Table 1) can reveal desirable and under- tive. A greater appreciation and consideration of po- performing combinations. Desirable combinations tential interactions between and among treatments February 2012 SUCKLING ET AL.: INSECT ERADICATION 9 that synergistically exploit Allee dynamics could en- Bloem, S., K. A. Bloem, and A. L. Knight. 1998. Oviposition hance the success and reduce costs of eradication by sterile codling moths and control of wild populations programs. with combined releases of sterile moths and egg parasi- toids. J. Entomol. Soc. B.C. 95: 99Ð109. Boettner, G. H., J. S. Elkinton, and C. J. Boettner. 2000. Effects of a biological control introduction on three non- Acknowledgments target native species of saturniid moths. Conserv. Biol. 14: This review was developed in conjunction with the “Ap- 1798Ð1806. plying population ecology to strategies for eradicating inva- Boone, C. K., B. H. Aukema, J. Bohlmann, A. L. Carroll, and sive forest insects” Working Group supported by the National K. F. Raffa. 2011. EfÞcacy of tree defense physiology Center for Ecological Analysis and Synthesis (http://www. varies with bark beetle population density: a basis for nceas.ucsb.edu/), a Center funded by NSF (Grant EF- positive feedback in eruptive species. Can. J. For. Res. 41: 0553768), the University of California, Santa Barbara, the 1174Ð1188. State of California and the U.S. Forest Service Eastern Forest Borden, J. H. 1989. Semiochemicals and bark beetle popu- Environmental Threat Assessment Center, Asheville, NC. lations: exploitation of natural phenomena by pest man- We thank our working group colleagues Julie Blackwood, agement strategists. Holarct. Ecol. 12: 501Ð510. 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