Invasive insect pests are a significant and accelerating threat to agricultural productivity, they degrade wilderness areas, and reduce quality of life in urban zones. Introduction biological control, the introduction, release, and establishment of host-specific efficacious natural enemies, is an effective management tool for permanently suppressing invasive pest populations over vast areas, often to levels that may no longer cause economic or environmental damage. However, introduction biological control programs are reactive: they are only initiated after an invasive pest has established, spread, and is causing damage that requires mitigation. Host specificity and host range testing of natural enemies for use in an introduction biological control program against an invasive pest can take years to complete. During this time, the target pest population continues to increase, invades new areas, and inflicts damage. Proactive biological control research programs identify prior to their establishment pest species that have high invasion potential and are likely to cause economic or environmental damage once established. Natural enemies are selected, screened, and if sufficiently host-specific, approved for release in advance of the anticipated establishment of the target pest. Following detection of the target pest and determination that incipient populations cannot be eradicated, natural enemies already approved for release are liberated into infested areas. This proactive approach to introduction biological control could significantly reduce project development time post-invasion, thereby lessening opportunities for pest populations to build, spread, and cause damage.
Invasive species are non-native organisms that have been deliberately or inadvertently introduced into areas outside of their native range by human activities, where, following permanent establishment, proliferation, and spread, cause adverse economic, ecological, and human-health impacts. Invasive non-native species are a perennial problem requiring escalating levels of human management to abate (Pyšek et al. 2020). Drivers for translocating species from their native range to new areas where they may become invasive include increasing volumes of exported and imported materials, human mobility, and land degradation (Seebans et al. 2018). Expanding agricultural and horticultural enterprises are also significant contributors (Paini et al. 2016; Seebans et al. 2017). Alarmingly, there appears to be no slowing of human-mediated movement of non-native species into new areas (Seebans et al. 2017). Increasing trade and tourism allow access to new regions that were previously isolated and enhanced accessibility is providing opportunities for additional species with invasive potential to be translocated from new source areas (Seebans et al. 2018).
To mitigate introduction risks, inspections of arriving goods and personal baggage at ports of entry are standard procedures for national biosecurity programs (Turner et al. 2021). However, given the vast volumes of goods moved by trade and tourism only a tiny fraction of material is inspected (Turner et al. 2021). Failure to inspect enables incursions by “unseen arrivals” that may be species known to be problematic (Turner et al. 2020) or “emerging alien species” which are relatively unknown species that have nascent invasion potential (Seebans et al. 2018). To avoid negative connotations associated with the noun “alien” the adjective “invasive” is used here to denote the non-native origin of the pest and its propensity for spreading and causing damage. Identifying “emerging invasive species” a priori is extremely challenging as there is likely no invasion history associated with the incipient pest (Paini et al. 2016), or it may be an unknown species new to science at the time of invasion (Hoddle et al. 2006).
Biosecurity preparedness relies in part on “horizon scanning” studies that attempt to identify “lurkers on the threshold” (Hoddle 2006) or “door-knocker” species (Seebans et al. 2018) that have high incursion risk, and are likely capable of causing significant negative impacts following establishment and spread (Hoddle 2006; Seebans et al. 2018). With respect to “horizon scanning” for potential invasive species, “invasion bridgeheads” (Lombaert et al. 2010) or “invasion hubs” (Florance et al. 2011), established invasive populations that act as sources of colonists for additional or secondary invasion events (Bertelsmeier et al. 2018) have been identified as predictable progenitors for intra- (Paini et al. 2010) and inter-continental spread of invasive pests (Correa et al. 2019).
Amongst invasive species, some of the smallest and most difficult to detect are insects and mites, which can cause significant adverse impacts following establishment in non-native habitats (Boubou et al. 2012; Turner et al. 2021). Drivers for herbivorous arthropod (i.e., insects and mites) movement are strongly linked to trade in live plants (Liebhold et al. 2012), which is also a source of invasive weed species (Bradley et al 2012) and plant pathogens (Liebhold et al. 2012), and agricultural exports (Paini et al. 2016; Lu et al. 2021). Examples of some important arthropod invaders that have undergone range expansion via invasion bridgeheads include: Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae) (Luo and Agnarsson 2018), brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) (Cesari et al. 2017; Valentine et al. 2017), glassy-winged sharpshooter, Homalodisca vitripennis (Germar) (Hemiptera: Cicadellidae) (Hoddle and Morgan 2022), obscure mealybug, Pseudococcus viburni (Signoret) (Hemiptera: Pseudoccidae) (Correa et al. 2019), palm weevils, Rhynchophorus spp. (Coleoptera: Curculionidae) (Rugman-Jones et al. 2013), spotted lanternfly, Lycorma delicatula (White) (Hemiptera: Fulgoridae) (Du et al. 2021), red tomato spider mite, Tetranychus evansi Baker and Pritchard (Trombidiformes: Tetranychidae) (Boubou et al. 2012), and western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) (Yang et al. 2012; Reitz et al. 2020).
“Horizon scans” have highlighted “invasion bridgeheads” as an important phenomenon driving the biogeography, and regional, national, and international flow of invasive species (Bertelsmeier et al. 2018; Bertelsmeier and Ollier 2021; Ricciardi et al. 2021). Collaborative identification and mitigation of invasion bridgeheads (Ricciardi et al. 2021) may lessen threats to agricultural trade partners (Paini et al. 2016; Huron et al. 2022) and possibly aid in the identification of native range areas from which invasive populations originated (Luo and Agnarsson 2018; Correa et al. 2019). This, in turn, may enable location of natural enemies adapted to invasive genotypes that originated in the native or invaded range, and to climatic conditions in invaded areas that could be used in introduction biological control programs for managing pest populations (Lara and Hoddle 2015).
Introduction biological control
Introduction biological control, also referred to as classical or importation biological control, is a tool that can be used for managing damaging populations of invasive pests, and is most commonly employed against non-native pest insects and weeds (Hoddle et al. 2021). Specifically, introduction biological control is the deliberate collection, importation, release, and establishment of host-specific natural enemies (e.g., predators, parasitoids, or entomopathogens for arthropods, or herbivorous arthropods and plant pathogens for weeds) by qualified biological control scientists with the intent of suppressing pest populations to less damaging densities. Introduction biological control employs an upper trophic level organism (e.g., a parasitoid) to manage an invasive pest (e.g., herbivorous insect) occupying a lower trophic level. Introduction biological control programs are meticulously planned invasion projects in which a myriad of steps are carefully managed. These steps can include careful selection of a source population from within a circumscribed geographical location, management of the genetic constitution of populations of released natural enemies, precise records on numbers of individuals released and frequency of introductions, and judicious choice of release locations and times of year releases are made (Hoddle and Morgan 2022; Hoddle et al. 2022a). van Driesche et al. (2008) and Hoddle et al. (2021) provide overviews on the steps involved in developing introduction biological control programs.
Introduction biological control programs constitute a reactive management response to an invasive pest after it has become well-established, widespread, and problematic. Implementation is a multi-year process, during which time target pest populations continue to increase, spread, and inflict damage. The D. citri invasion into California, USA is an illustrative example of the time needed to develop an introduction biological control program for an invasive agricultural pest.
Case study: a reactive response to an invasion—development of an introduction biological control program for Asian citrus psyllid, Diaphorina citri, in California, USA
Diaphorina citri (Fig. 1a), native to the Indian subcontinent, is arguably the most destructive invasive pest affecting global citrus production because of its ability to acquire and vector a bacterium, Candidatus Liberibacter asiaticus Jagoueix et al. (CLas), which causes a lethal citrus disease known as huanglongbing or citrus greening (Fig. 1b) (Bové 2006; Grafton-Cardwell et al. 2013). In North America, D. citri established its first “invasion bridgehead” in Florida, USA in 1998 (Halbert and Manjunath 2004) and CLas was first identified there in 2005 (Farnsworth et al. 2014). The subsequent economic impacts of D. citri-CLas on the Florida citrus industry have been considerable (Alvarez et al. 2016).
A second North American D. citri bridgehead was later reported from México in 2002, and importantly, for California, the presence of D. citri was confirmed in Tijuana, Baja California México in 2008. Tijuana is a large populous border city situated on the California-Mexican border. In 2009, CLas was officially detected in México (Cortez-Mondaca et al. 2009). In 2008, D. citri was detected ~ 10 km north of Tijuana when established populations were found in San Diego County in California. Shortly thereafter, a larger and more widespread D. citri infestation was found in Los Angeles County (~ 120 km north of San Diego County) which was indicative of an earlier incursion event that had gone undetected (Hoddle et al. 2022a). In 2012, the first CLas infected citrus tree was discovered in Los Angeles County California. The threat to California’s ~ $7 billlion USD per year citrus industry from D. citri-CLas had now been realized, and the concern was would impacts be as severe as those observed in Florida (Hoddle et al. 2022a)?
The initial response plan to manage D. citri in California was insecticide-focused with the goal of containment and eradication. This program was, however, abandoned due to an inability to contain D. citri as it continued to spread over larger areas, with infested areas requiring repeat treatments, public disquiet with insecticide applications, and cost (> $4.7 million USD) (Hoddle and Pandey 2014). The abandonment of insecticide application campaigns provided an opportunity to consider an alternative reactive response for D. citri management, introduction biological control, which commenced in 2010, two years after D. citri establishment was confirmed in California (Hoddle and Pandey 2014; Bistline-East et al. 2015; Hoddle et al. 2022a). Frustratingly, the introduction biological control project was not supported until insecticide management efforts ceased. The rationale for this decision was due to concern that a concurrent biological control program would detract support for insecticide use which may have resulted in refusals to participate in spray programs if biological control was viewed more favorably as an alternative management tactic.
The biological control program for D. citri sourced two species of nymphal parasitoid, Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae) (Fig. 1c) and Diaphorencyrtus aligarhensis (Shafee, Alam and Agarwal) (Hymenoptera: Encyrtidae) (Fig. 1d) from Punjab Pakistan, part of the putative native range of this pest, and an area with a ~ 70% climate match with major citrus production areas in California’s Central Valley (Hoddle et al. 2022a). Following release, approximately three years after detection of D. citri in California (Fig. 1e), T. radiata established readily, spread quickly, and D. citri densities declined by > 70% after releases began (Hoddle et al. 2016; Kistner et al. 2016; Milosavljević et al. 2021). Diaphorencyrtus aligarhensis, collected at the same time as T. radiata, was evaluated for safety, and was then approved for release by Federal regulatory authorities approximately six years after D. citri was detected in California (Fig. 1e). This parasitoid failed to establish despite releases of > 700,000 individuals (Hoddle et al. 2022a; Milosavljević et al. 2022).
Given that D. citri invasion bridgeheads existed in Florida (1998) and México (2002) and that this insect is a notorious global citrus pest with high invasion potential, a retrospective question that deserves consideration is: “Could advance D. citri biological control preparedness in California have been better?” In hindsight, proactive actions to prepare an introduction biological control program in advance of the anticipated incursion and establishment of D. citri in California would have been justified. Such activity, if undertaken when D. citri invasion bridgeheads had been identified in Florida and México, would have permitted a more rapid biological control response to managing the D. citri incursion in California which could have slowed spread and reduced pest densities, with a possible concomitant reduction in incidences of vector-disseminated CLas. Having host-specific natural enemies already selected and permitted for release prior to the establishment of a target invasive pest is the core concept underlying proactive biological control (Hoddle et al. 2018).
Proactive biological control research: a deep dive into development and application
Selecting targets for proactive biological control research programs can be achieved by conducting “horizon scans” for “door knocker” species that have already established invasion bridgeheads and are exhibiting a propensity for spread. In California, for example, around 9–10 new macroinvertebrate species (i.e., insects, mites, spiders, terrestrial crustaceans, mollusks) establish per year. The majority of these non-native organisms are primarily plant feeding insects, of which, approximately three or so each year will become pests requiring management (Dowell et al. 2016). Importantly, approximately 44% of invaders that establish in California originate from invasion bridgeheads established elsewhere in the USA and Canada (Dowell et al. 2016). Tracking establishment and spread data is a prudent practice for identifying new invasive threats. In this regard, spotted lanternfly, L. delicatula, is a serious threat of spreading within North America and poses a significant invasion risk to other countries (Wakie et al. 2020; Huron et al. 2022).
Horizon scans for known “door knocker” species
Lycorma delicatula, native to China, established in South Korea in 2004 (Park et al. 2013), in Japan in 2009 (Nakashita et al. 2022), and the northeast USA in 2014 (Urban 2019). This polyphagous lanternfly is a pest of perennial agricultural crops (i.e., grapes and walnuts) and it was a target for introduction biological control in South Korea with an egg parasitoid, Anastatus orientalis Yang and Choi (Hymenoptera: Eupelmidae), sourced from China (Seo et al. 2019). Subsequently, A. orientalis sourced directly from China, was imported into the USA as a potential biological control agent of L. delicatula. Because L. delicatula is widely established on the east coast of the USA and numerous invasion bridgeheads are forming in the Midwest (e.g., Indiana), “horizon scanning” determined that this pest poses a significant invasion threat to California specialty crops (e.g., nuts, grapes, kiwifruit). Consequently, A. orientalis host range and host specificity were assessed prior to established populations of L. delicatula being detected in California (Gómez Marco et al. 2023).
Similar proactive biological control research efforts were initiated against H. vitripennis by New Zealand (Groenteman et al. 2015) and Australia (Rathe et al. 2012; 2014) and for H. halys by New Zealand (Charles et al. 2019). Homalodisca vitripennis, native to southeastern USA and northeast México, invaded California sometime in the 1980’s and became a significant pest because it vectored a xylem-limited bacterium, Xylella fastidiosa Wells et al. (Xanthomonadaceae), the causative agent of the lethal grape malady, Pierce’s disease (Hoddle and Morgan 2022). Homalodisca vitripennis was identified as a significant incursion threat for New Zealand and Australia following establishment of invasion bridgeheads in the South Pacific. The first bridgehead established in French Polynesia (1999) possibly due to importation of infested nursery stock from California. Established H. vitripennis populations were then detected in Hawaii (2004), Easter Island (2005) and the Cook Islands (2007) (Hoddle and Morgan 2022). Movement of live plants infested with H. vitripennis from areas with invasion bridgeheads was the most likely conduit for translocating this pest to new areas within the South Pacific (Petit et al. 2009). Consequently, high levels of tourism between New Zealand and Australia with H. vitripennis infested areas (e.g., French Polynesia) was a recognized incursion pathway for those two countries. Additionally, ecological niche modeling indicated New Zealand and Australia had climates suitable for H. vitripennis to persist year round, should it establish, thereby potentially threatening important agricultural industries such as wine grape production (Hoddle 2004a).
In the absence of effective natural enemies, H. vitripennis populations reached astounding densities in French Polynesia (Grandgirard et al. 2007a, 2008, 2009). An introduction biological control program targeting H. vitripennis in French Polynesia with an egg parasitoid, Cosmocomoidea ashmeadi (Girault) (Hymenoptera: Mymaridae), provided rapid and spectacular suppression of this pest within seven months of release (Grandgirard et al. 2008; 2009). High and persistent levels of suppression by C. ashmeadi in all invaded regions in the South Pacific resulted in cessation of H. vitripennis spread throughout this area (Weber et al. 2021; Wyckhuys et al. 2021; Hoddle and Morgan 2022). The success of this program significantly reduced incursion risks to New Zealand and Australia from areas with established H. vitripennis populations because the threat likelihood from illegal movement of infested plant material (Hoddle and Morgan 2022) or accidental transportation of adults in aircraft (Rathe et al. 2015) was diminished. Cosmocomoidea ashmeadi is host-specific to members of Proconiini (Boyd and Hoddle 2007; Grandgirard et al. 2007b), a cicadellid tribe restricted to the Americas. Because species of Proconiini do not naturally occur in New Zealand (and Australia), Charles (2012) proposed that C. ashmeadi should not be subjected to non-target host testing prior to use in New Zealand should this parasitoid be needed for biological control of H. vitripennis.
Brown marmorated stink bug, H. halys, native to China, Japan, Korea, and Taiwan has successfully invaded Canada, the USA, Europe, and Chile (Charles et al. 2019). This polyphagous pest is a significant threat to horticultural industries, such as kiwifruit, grapes, and apples, which are major crops in New Zealand (Fraser et al. 2017; Charles et al. 2019). Ecological niche modeling indicates that H. halys has significant capacity to continue to expand its range and this pest has been intercepted numerous times entering New Zealand, indicating that it may be prudent to prepare in advance for the eventual establishment of this pest (Fraser et al. 2017; Avila and Charles 2018; Yanow et al. 2021). The egg parasitoid, Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae), a natural enemy of H. halys, has been proactively screened and approved for use in a proactive biological control program against this pest in New Zealand should it establish (Charles et al. 2019). Even though evidence of attack to New Zealand native species exists (Saunders et al. 2021) the probable benefits from biological control of H. halys with T. japonicus were determined to outweigh risks to non-target species (Charles et al. 2019).
Horizon scans for “wild cards” and “emerging invasive species”
Arguably, a more difficult challenge for developing a proactive biological control program would be identification of “wild card species” (i.e., unknown or unpredictable entities) that fall into the “emerging invasive species” category prior to them establishing “invasion bridgeheads” and becoming obvious “door knockers”. Emerging invasive insect threats, for example, could be recognized pests associated with agricultural crops that have high export volumes from source regions (e.g., Lu et al. 2021), or unknown or little studied pest species associated with a crop that is grown in the crop’s native or naturalized range, and from where there are high export volumes, and this crop, especially in the native range, has high levels of little studied native or endemic biodiversity associated with it (Hoddle 2004b; 2006). Avocado fruit, Persea americana Miller (Lauraceae) exports from countries where this plant is native [e.g., México and Guatemala (Chanderbali et al. 2013)], naturalized in wilderness areas [e.g., Perú (Gray 1930)] where Lauraceae and Persea are well represented (León 2006) and specialist fruit feeding insects are likely present, or imports were restricted because of previous interceptions of fruit infested with quarantine-regulated pests that are avocado fruit specialists [e.g., Colombia (Hoddle et al. 2022b)] are possible sources of invasive avocado fruit pests. The previous scenarios illustrate three possible incursion routes by “wild card” or emergent invasive species: (1) high export volumes of fruit from regions where the crop is native or naturalized that may be infested with known species of fruit feeding pests, (2) unexpected “wild card” introductions by unknown or relatively poorly studied native or endemic pest species associated with fruit in native or naturalized regions, and (3) previous repeated interceptions of specialized fruit feeding pest species that has resulted in revocation of export privileges.
Avocados are an iconic California specialty crop with an annual value of approximately $328-$411 million USD (CAC 2022). Importantly, year round imports of fresh avocado fruit from México and Colombia and during March-October from Perú increases the likelihood of undetected incursions of fruit pests aligning with favorable conditions for establishment in California (i.e., suitable weather and availability of fruit stages vulnerable to attack). Even though these events co-aligning are probably very low, the “law of large numbers” states that a rare event with a low probability of occurrence in a small number of trials has a high probability of occurrence in a large number of trials (Shermer 2004; Hand 2014). Therefore, rare events, for example pest introductions resulting in establishment, may not be so uncommon when the number of times the rare event could happen is very large, such as the importation of hundreds of millions of avocado fruit from areas with known fruit feeding pests over long periods of time.
Two notorious specialist avocado fruit pests of quarantine importance for the USA are the avocado seed moth Stenoma catenifer Walsingham (Lepidoptera: Elachistidae) native to México, Perú, and Colombia (invasive in the Galápagos Islands), and the large avocado seed weevil, Heilipus lauri Boheman (Coleoptera: Curculionidae), native to México, absent in Péru, invasive in Colombia. Given the notoriety of these avocado fruit-feeding pests, it is surprising that relatively little is known about their biology, ecology and behavior, and arguably monitoring and management plans are not well developed (Castañada-Vildózola et al. 2013; Hoddle and Parra 2013). California currently lacks specialist avocado fruit-feeding pests and establishment of fruit-feeding moths and weevils, for example, would cause significant industry upheaval.
A proactive approach to managing the threat posed by S. catenifer has resulted in the development of natural enemy inventories and life table studies documenting identities and impacts of natural enemy species that could be used in future introduction biological control programs (Hoddle and Hoddle 2008a, b, c, 2012). Additionally, the elucidation and optimization of field use of the moth’s sex pheromone, an important detection and monitoring tool, has been completed (Hoddle et al. 2009a; 2011). A significant by-product of this work was the identification of previously unknown and undescribed pest species associated with avocado fruit (and their natural enemies) that could pose “wild card” incursion risks and records of first associations of described species with larval host foods (Hoddle 2008; Hoddle and Hoddle 2008c; Adamski and Hoddle 2009; Hoddle et al. 2009b; Brown and Hoddle 2010; Hoddle and Brown 2010; Gilligan et al. 2011).
Theoretically, should S. catenifer (or one of the discovered “wild card” species) be discovered in California tomorrow, an introduction biological control program could start rapidly as the groundwork on candidate natural enemy species in the native range has been completed. A similar proactive program is currently being developed for H. lauri to better position the California avocado industry (and production areas in Florida and Hawaii) should an incursion by this fruit pest result in establishment (Hoddle et al. 2022b,c).
A similar in-the-field approach to assess pestiferousness and invasion risks posed by little studied or unknown insect species (and plant pathogens) can be accomplished by surveying trees that are planted outside of their native ranges in botanic gardens, arboreta, as ornamentals in urban areas, or deliberately planted for observations in carefully designed “garden” experiments (Rathe et al. 2014; Groenteman et al. 2015; Roques et al 2015; Barham 2016; Popkin 2020; DiGirolomo et al. 2022). This proactive approach attempts to identity and forecast potential invasion threats posed by herbivorous insects ahead of possible future incursions into at risk areas. For example, a group of 23 European nations have established plantings of native European trees in North America, Asia, and South Africa, possible source areas of invasive pests, to identify phytophagous insect species from different regions of the world that will attack these trees (Popkin 2020).
Data on insect identities can be a significant challenge for sentinel plant studies (Roques et al. 2015) and attack severity, when coupled together with pest and host plant phenological data, may collectively help identify future potential invasive pest species. In addition to identification of potential pest species, supplemental research would identify natural enemy species associated with key pests of concern, the life stages attacked, and quantification of impacts (Rathe et al. 2014). Having these types of data on natural enemy species in-hand prior to a pest invasion would have two advantages. First, it could significantly reduce the time needed to develop introduction biological control programs as natural enemy identities and possible levels of control would be known. Second, these data may identify natural enemy species that have potential for self-introductions into new areas should they accompany pestiferous hosts during the invasion process. Unintentional introductions in this manner exceed the number of natural enemy species deliberately introduced into areas in support of introduction biological control programs (Weber et al. 2021). Discovery of adventive natural enemy species has raised concerns over population-level impacts on non-target species, which has led to increased research activity on this phenomena (Weber et al. 2021) and proactive biological control research may ease concerns associated with potential non-target impacts by self-introduced natural enemy species.
Conducting horizon scans using online platforms, networks, professional meetings, and incursion monitoring programs
Online virtual tools that distribute information on new and emerging phytosanitary threats are an additional way to conduct “horizon scans” on a global level for potential invasive pests that may be suitable targets for proactive biological control research. PestLens (https://pestlens.info/), an early warning system, produces weekly email notifications that are distributed automatically to subscribers. The information reported by PestLens that are relevant to proactive biological control research include descriptions and identification of new pest species, updates on pest distribution records (i.e., notification of invasion bridgeheads), new host records, notifications of significant pest outbreaks, and reports of new insect-vector relationships. Registered PestLens users can access a searchable archive of first records for pests of interest and contribute new information on pest threats to the site that may come from site visits and field work, collaborative projects with colleagues, or new information on known or emerging pest threats presented at professional meetings. The International Plant Sentinel Network (https://www.bgci.org/our-work/networks/ipsn/) is an early warning system for identifying emerging tree pests and aims to facilitate collaborative efforts amongst arboreta, botanical gardens, regional, national, and international plant protection organizations and research scientists (Barham 2016; Barham et al. 2016). Online community science platforms, like iNaturalist, may also be useful resources for alerts of new reports on “door knocker” species. International symposia are excellent sources for new information on emerging invasive threats that have not yet entered the peer-reviewed scientific literature.
Pest surveillance programs may be additional sources of information that result from near daily “horizon scanning” activities. Detections of pests, especially in monitoring traps deployed by regulatory agencies, would be indicative of incursions by live vagile adults that may result in establishment. For example, the California Department of Food and Agricultural (CDFA) runs statewide pest detection and emergency projects operations that are focused on early detection and rapid eradication of serious agricultural pests (i.e., insects and plant diseases) should incipient populations be detected (https://www.cdfa.ca.gov/plant/pdep/). Additionally, 16 border protection stations that monitor and inspect vehicles entering California along major highways in the north from Oregon and east of the state from Nevada and Arizona, USA. More than 20 million private vehicles and seven million commercial vehicles are inspected annually for plant material (i.e., fruit, vegetables, plants, and firewood) that are potentially infested with actionable pest species (https://www.cdfa.ca.gov/plant/pe/ExteriorExclusion/borders.html). Frequent detections of species with known or suspected invasion potential by border protection programs may warrant consideration as potential targets for proactive biological control research.
What if proactive biological control research fails to identify host-specific natural enemies for a target pest?
A possible outcome resulting from proactive biological control research programs is the failure to identify natural enemy species that exhibit sufficient host specificity for future use in an introduction biological control project. This situation may be relevant for the proactive biological control program targeting L. delicatula in California with A. orientalis (Gomez-Marco et al. 2023). Host range testing indicated that A. orientalis is likely polyphagous and can successfully parasitize and develop in host species belonging to at least two different orders (Hemiptera and Lepidoptera) and seven families (Coreidae, Erebidae, Fulgoridae, Lasiocampidae, Pentatomidae, Saturniidae and Sphingidae). The previously unknown polyphagy of A. orientalis led to the conclusion that A. orientalis has a very broad host range and consideration of use in an introduction biological control program targeting L. delicatula should be viewed with extreme caution (Gomez-Marco et al. 2023). Despite this negative outcome, such findings allow research priorities for managing “door knocker” pests to be moved elsewhere. In California, proactive biological control research for L. delicatula is focusing on assessing possible levels of naturally occurring biotic resistance from resident (i.e., native and introduced) species of Anastatus. Additionally, it is likely that integrated pest management approaches that rely more heavily on control tactics other than biological control will be warranted and may need to be prioritized for L. delicatula management.
Proactive biological control research should be funded as insurance programs
Funding and development of proactive biological control research programs is analogous to buying insurance. The owners of insurance policies hope not to need them but benefit from being holders when catastrophe strikes. Federal and state agencies responsible for developing biological control programs for managing invasive pests could enact funding programs as “insurance” against future pest threats to support proactive biological control research efforts. The CDFA Office of Pesticide Consultation and Analysis runs a proactive IPM (Integrated Pest Management) solutions program, of which proactive biological control research is a component eligible for competitive funding via a grant application and review process. The goal of the program is to identify, anticipate, and prepare in advance for the arrival into California of invasive pests and to have management strategies in place that can be rapidly implemented should established pest populations be detected (https://www.cdfa.ca.gov/oefi/opca/proactive-ipm.html). Since its inception in 2019, this program has sponsored research on L. delicatula, H. lauri, swede midge, Contarina nasturtii (Keiffer) (Diptera: Cecidomyiidae), South American tomato pinworm, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae), emerald ash borer, Agrilus planipennis Fairmarie (Coleoptera: Buprestidae), and cotton seed bug, Oxycarenus hyalinipennis (Costa) (Hemiptera: Lygaeidae).
Development of introduction biological control research programs to manage invasions are reactive and can take years to develop. To reduce development and implementation times, proactive biological control research programs aim to identify potential invasive pests that may be good targets for introduction biological control prior to pest establishment in at risk areas. Natural enemies are identified, screened for safety, and approved for release prior to detection of established non-eradicable target pest populations (Fig. 2). In some instances, host-specific natural enemies may not be identified, and, in these cases, resources may need to be redirected to the development of management programs that rely more heavily on alternative pest control options. Investment in proactive biological control research can be viewed as being analogous to an insurance policy, excellent to have, but something policy holders hope will not be needed. Proactive biological control research is a new twist on a classic approach to managing invasive pests.
Adamski D, Hoddle MS (2009) A new Holcocera Clemens from guatemala and redescription of H. iceryaeella (Riley) from the United States (Lepidoptera: Coleophoridae: Blastobasinae: Holcocerini): two congeners with incidental preference for avocado. Proc Entomol Soc Wash 111:254–262
Alvarez S, Rohrig E, Solís D, Thomas MH (2016) Citrus greening disease (Huanglongbing) in Florida: economic impact, management, and potential for biological control. Agric Res 5:109–118
Avila GA, Charles JG (2018) Modelling the potential geographic distribution of Trissolcus japonicus: a biological control agent of the brown marmorated stink bug, Halyomorpha halys. BioControl 63:505–518
Barham E (2016) The unique role of sentinel trees, botanic gardens, and arboreta in safeguarding global plant health. Plant Biosyst 150:377–380
Barham E, Sharrock S, Lane C, Baker R (2016) The International Plant Sentinel Network: a tool for regional and national plant protection organizations. EPPO Bull 46:156–162
Bertelsmeier C, Ollier S (2021) Bridgehead effects distort global flows of alien species. Divers Distrib 27:2180–2189
Bertelsmeier C, Ollier S, Leibhold AM, Brockerhoff EG, Ward D, Keller L (2018) Recurrent bridgehead effects accelerate global alien ant spread. Proc Nat Acad Sci 115:5486–5491
Bistline-East A, Pandey R, Kececi M, Hoddle MS (2015) Host range testing of Diaphorencyrtus aligarhensis (Hymenoptera: Encyrtidae) for use in classical biological control of Diaphorina citri (Hemiptera: Liviidae) in California. J Econ Entomol 108:940–950
Boubou A, Migeon A, Roderick GK, Auger P, Cornuet J-M, Magalhães S, Navajas M (2012) Test of colonization scenarios reveals complex invasion history of the red tomato spider mite Tetranychus evansi. PLoS ONE 7(4):e35601
Bové JM (2006) Huanglongbing: a destructive, newly-emerging, century-old disease of citrus. J Plant Pathol 88:7–37
Boyd EA, Hoddle MS (2007) Host specificity testing of Gonatocerus spp. egg parasitoids used in a classical biological control program against Homalodisca vitripennis: a retrospective analysis for non-target impacts in southern California. Biol Control 43:56–70
Bradley BA, Blumenthal DM, Early R, Grosholz ED, Lawler JJ, Miller LP, Sorte CJB, D’Antonio CM, Diez JM, Dukes JS, Ibanez I, Olden JD (2012) Global change, global trade, and the next wave of plant invasions. Front Ecol Environ 10:20–28
Brown JL, Hoddle MS (2010) A new species of Histura Razowski (Lepidoptera: Tortricidae: Polyorthini) from Guatemala attacking avocados (Persea americana) (Lauraceae). Proc Entomol Soc Wash 112:10–21
CAC (2022) California Avocado Commission annual Report 2021. https://www.californiaavocadogrowers.com/sites/default/files/2021-CAC-Annual-Report-FINAL.pdf. Accessed 30 April 2023
Castañeda-Vildózola A, Equihua-Martínez A, Peña JE (2013) Avocado weevils of the genus Heilipus. In: Peña JE (ed) Potential invasive pests of agricultural crops. CABI, Wallingford, pp 35–47
Cesari M, Maistrello L, Piemontese L, Bonini R, Dioli P, Lee W, Park C-G, Partsinevelos GK, Rebecchi L, Guidetti R (2017) Genetic diversity of the brown marmorated stink bug Halyomorpha halys in the invaded territories of Europe and its pattern of diffusion in Italy. Biol Invasions 20:1073–1092
Chanderbali AS, Soltis DE, Soltis PS, Wolstenholme BN (2013) Taxonomy and botany. In: Schaffer B, Wolstenholme BN, Whiley AW (eds) The avocado—botany production and uses, 2nd edn. CABI, Wallingford, pp 31–50
Charles JG (2012) Assessing non-target impacts of classical biological control agents: is host testing always necessary? BioControl 57:619–626
Charles JG, Avila GA, Hoelmer KA, Hunt S, Gardner-Gee R, MacDonald F, Davis V (2019) Experimental assessment of the biosafety of Trissolcus japonicus in New Zealand, prior to the anticipated arrival of the invasive pest Halyomorpha halys. BioControl 64:367–379
Correa MCG, Palero F, Malausa T, Crochard D, Zaviezo T, Lombaert E (2019) European bridgehead effect in worldwide invasion of the obscure mealybug. Biol Invasions 21:123–136
Cortez-Mondaca E, Lugo-Angulo NE, Pérez-Márquez J, Apodaca-Sánchez MA (2009) Primer reporte de enemigos naturales y parasitismom sobre Diaphorina citri Kuwayama en Sinaloa México. Southwestern Entomol 35:113–116
DiGirolomo MF, Bohne MJ, Dodds KJ, Gapinski AT, DelRosso JS, Charap JG, Evans SC (2022) Utilizing urban arboreta for detection of native and non-native wood-inhabiting beetles. Agric for Entomol 24:72–96
Dowell RV, Gill RJ, Jeske DR, Hoddle MS (2016) Exotic terrestrial macro-invertebrate invaders in California from 1700 to 2010: an analysis of records. CA Acad Sci Series 4(63):63–157
Du Z, Wu Y, Chen Z, Cao L, Ishikawa T, Kamitani S, Sota T, Song F, Tian L, Cai W, Li H (2021) Global phylogeography and invasion history of the spotted lanternfly revealed by mitochondrial phylogenomics. Evol Appl 14:915–930
Farnsworth DK, Grogan A, van Bruggen AHC, Moss CB (2014) The potential economic cost and response to greening in Florida. Choices 29:1–6
Florance D, Webb JK, Dempster T, Kearney MR, Worthing A, Letnic M (2011) Excluding access to invasion hubs can contain the spread of an invasive vertebrate. Proc R Soc B 278:2900–2908
Fraser D, Kumar S, Aguilar G (2017) Mapping the potential global range of the brown marmorated stink bug, Halyomorpha halys, with particular reference to New Zealand. Climate 5:75
Gilligan TM, Brown JW, Hoddle MS (2011) A new avocado pest in Central America (Lepidoptera: Tortricidae) with a key to Lepidoptera larvae threatening avocados in California. Zootaxa 3137:31–45
Gómez MF, Yanega D, Ruiz M, Hoddle MS (2023) Proactive biological control of Lycorma delicatula (Hemiptera: Fulgoridae) in California (U.S.): host range testing of Anastatus orientalis (Hymenoptera: Eupelmidae). Front Ins Sci 3:1134889
Grafton-Cardwell EE, Stelinski LL, Stansly PA (2013) Biology and management of Asian citrus psyllid, vector of the huanglongbing pathogens. Ann Rev Entomol 58:413–432
Grandgirard J, Hoddle MS, Triapitsyn SV, Petit JN, Roderick GK, Davies N (2007a) First records of Gonatocerus dolichocherus Ashmead, Palaeoneura sp., Anagrus sp. (Hymenoptera: Mymaridae) and Centrodora sp. (Hymenoptera: Aphelinidae) in French Polynesia, with notes on egg parasitism of the glassy-winged sharpshooter, Homalodisca vitripennis (Germar) (Hemiptera: Cicadellidae). Pan Pac Entomol 83:177–184
Grandgirard J, Hoddle MS, Petit JN, Percy DM, Roderick GK, Davies N (2007b) Pre-introductory risk assessment studies of Gonatocerus ashmeadi (Hymenoptera: Mymaridae) for use as a classical biological control agent against Homalodisca vitripennis (Hemiptera: Cicadellidae) in the Society Islands of French Polynesia. Biocontrol Sci Tech 17:809–822
Grandgirard J, Hoddle MS, Petit JN, Roderick GK, Davies N (2008) Engineering an invasion: classical biological control of the glassy-winged sharpshooter, Homalodisca vitripennis, by the egg parasitoid Gonatocerus ashmeadi in Tahiti and Moorea, French Polynesia. Biol Invasions 10:135–148
Grandgirard J, Hoddle MS, Petit JN, Roderick GK, Davies N (2009) Classical biological control of the glassy-winged sharpshooter, Homalodisca vitripennis, by the egg parasitoid Gonatocerus ashmeadi in the Society, Marquesas, and Austral archipelagos of French Polynesia. Biol Control 48:155–163
Gray RH (1930) Avocados in Peru. Cal Avo Soc Yearbook 15:130–131
Groenteman R, Forgie SA, Hoddle MS, Ward DF, Goeke DF, Anand N (2015) Assessing invasion threats: novel insect-pathogen-natural enemy associations with native New Zealand plants in southern California. Biol Invasions 17:1299–1305
Halbert SE, Manjunath KL (2004) Asian citrus psyllid (Sternorrhyncha: Psyllidae) and greening disease of citrus: A literature review and assessment of risk in Florida. Fla Entomol 87:330–353
Hand DJ (2014) The improbability principle: why coincidences, miracles, and rare events happen every day. Scientific American/Farrar Straus and Giroux, New York
Hoddle MS (2004a) The potential adventive geographic range of glassy-winged sharpshooter, Homalodisca coagulata and the grape pathogen Xylella fastidiosa: implications for California and other grape growing regions of the world. Crop Prot 23:691–699
Hoddle MS (2004b) Invasions of leaf feeding arthropods: why are so many new pests attacking California-grown avocados? Cal Avo Soc Yearbook 87:65–81
Hoddle MS (2006) Lurkers on the threshold: potential new fruit pests for California avocados. Cal Avo Soc Yearbook 89:69–92
Hoddle MS (2008) First record of Asphondylia websteri (Diptera: Cecidomyiidae) infesting Hass avocados. Fla Entomol 91:501–503
Hoddle MS, Brown JL (2010) Lepidoptera associated with avocado fruit in Guatemala. Fla Entomol 93:649–650
Hoddle MS, Hoddle CD (2008a) Bioecology of Stenoma catenifer (Lepidoptera: Elachistidae) and associated larval parasitoids reared from Hass avocados in Guatemala. J Econ Entomol 101:692–698
Hoddle MS, Hoddle CD (2008b) Aspects of the field ecology of Stenoma catenifer (Lepidoptera: Elachistidae) infesting Hass avocados in Guatemala. Fla Entomol 91:693–694
Hoddle MS, Hoddle CD (2008c) Lepidoptera and associated parasitoids attacking Hass and non-Hass avocados in Guatemala. J Econ Entomol 101:1310–1316
Hoddle MS, Hoddle CD (2012) Surveys for Stenoma catenifer (Lepidoptera: Elachistidae) and associated parasitoids infesting avocados in Peru. J Econ Entomol 105:402–409
Hoddle MS, Para JRP (2013) Potential Lepidoptera pests associated with avocado fruit in parts of the home range of Persea americana. In: Peña JE (ed) Potential invasive pests of agricultural crops. CABI, Wallingford, pp 86–97
Hoddle MS, Morgan DJW (2022) Successful biological control of glassy-winged sharpshooter, Homalodisca vitripennis, in invaded regions. In: van Driesche RG, Winston RL, Perring TM, Lopez VM (eds) Contributions of classical biological control to the US food security, forestry, and biodiversity, FHAAST-2019–05. USDA Forest Service, Morgantown, West Virginia, pp 92–103. https://bugwoodcloud.org/resource/files/23194.pdf
Hoddle MS, Pandey R (2014) Host range testing of Tamarixia radiata (Hymenoptera: Eulophidae) sourced from the Punjab of Pakistan for classical biological control of Diaphorina citri (Hemiptera: Liviidae: Euphyllurinae: Diaphorinini) in California. J Econ Entomol 107:125–136
Hoddle MS, Nakahara S, Phillips PA (2006) Foreign exploration for Scirtothrips perseae Nakahara (Thysanoptera: Thripidae) and associated natural enemies on avocado (Persea americana Miller). Biol Control 24:251–265
Hoddle MS, Millar JG, Hoddle CD, Zou Y, McElfresh JS (2009a) Synthesis and field evaluation of the sex pheromone of Stenoma catenifer (Lepidoptera: Elachistidae). J Econ Entomol 102:1460–1467
Hoddle MS, Mottern JL, Hoddle CD (2009b) Observations on Asphondylia websteri (Diptera: Cecidomyiidae) infesting Hass avocados in Guatemala. Fla Entomol 92:673–674
Hoddle MS, Millar JG, Hoddle CD, Zou Y, McElfresh JS, Lesch S (2011) Field optimization of the sex pheromone of Stenoma catenifer (Lepidoptera: Elachistidae): evaluation of lure types, trap height, male flight distances, and number of traps needed per avocado orchard for detection. Bull Entomol Res 101:145–152
Hoddle MS, Amrich R, Hoddle CD, Kistner EJ (2016) Where’s Tamarixia? Citrograph 7:64–66
Hoddle MS, Mace K, Steggall J (2018) Proactive biological control: a cost effective management option for invasive pests. Calif Agric 72:148–150
Hoddle MS, Lake EC, Minteer CR, Daane KM (2021) Importation biological control. In: Mason PG (ed) Biological control—global impacts, challenges and future directions of pest management. CSIRO Publishing, Victoria, pp 67–89
Hoddle MS, Hoddle CD, Morgan DJW, Milosavljević I (2022a) Successful biological control of Asian citrus psyllid, Diaphorina citri, in California. In: van Driesche RG, Winston RL, Perring TM, Lopez VM (eds) Contributions of classical biological control to the US food security, forestry, and biodiversity, FHAAST-2019–05. USDA Forest Service, Morgantown, West Virginia, USA, pp 127–143. https://bugwoodcloud.org/resource/files/23194.pdf
Hoddle MS, Hoddle CD, Milosavljević I, Estrada-Venegas EG, Equihua-Martínez A (2022b) Assessment of age, gender, mating status, and size on single and repeat flight capabilities of Heilipus lauri Boheman (Coleoptera: Curculionidae). J Ins Sci 22:3
Hoddle CD, Estrada-Venegas EG, Equihua-Martinez A, Millar JG, Halloran S, Hoddle MS (2022c) What do we know about Heilipus lauri, the large avocado seed weevil? CAPCA Adviser 25:52–56
Huron NA, Behm JE, Helmus MR (2022) Paninvasion severity assessment of a US grape pest to disrupt the global wine market. Comm Biol 5:655
Kistner EJ, Melhem N, Carpenter E, Castillo M, Hoddle MS (2016) Abiotic and biotic mortality factors affecting Asian citrus psyllid (Hemiptera: Liviidae) demographics in southern California. Ann Entomol Soc Am 109:860–871
Lara JR, Hoddle MS (2015) Past, present, and future: biological control of spider mites on California-grown avocados. In: Carrrillo D, de Moraes GJ, Peña JE (eds) Prospects for biological control of plant feeding mites and other harmful organisms, progress in biological control 19. Springer, Berlin, pp 271–308
León B (2006) Lauraceae endémicas del Perú. Revista Peruana De Biol 13:380s–388s
Liebhold AM, Brockerhoff EG, Garrett LJ, Parke JL, Britton KO (2012) Live plant imports: the major pathway for forest insect and pathogen invasions of the US. Front Ecol Environ 10:135–143
Lombaert E, Guillemaud T, Cornuet J-M, Malausa T, Facon B, Estoup A (2010) Bridgehead effect in the worldwide invasion of the biocontrol harlequin ladybird. PLoS ONE 5(3):e9743
Lu G, Zhao Z, Pan X (2021) Potential pest invasion risk posed by international sweet cherry trade. Food Energy Secur 10:e257
Luo Y, Agnarsson I (2018) Global mtDNA structure and hypothesized invasion history of a major pest of citrus, Diaphorina citri (Hemiptera: Liviidae). Ecol Evol 8:257–265
Milosavljević I, Morgan DJW, Massie RE, Hoddle MS (2021) Density dependent mortality, climate, and Argentine ants affect population dynamics of an invasive citrus pest, Diaphorina citri, and its specialist parasitoid, Tamarixia radiata, in southern California, USA. Biol Control 159:104627
Milosavljević I, Vankosky MA, Morgan DJW, Hoddle CD, Massie RE, Hoddle MS (2022) Post-release evaluation of Diaphorencyrtus aligarhensis (Hymenoptera: Encyrtidae) and Tamarixia radiata (Hymenoptera: Eulophidae) for biological control of Diaphorina citri (Hemiptera: Liviidae) in urban California, USA. Agronomy 12:583
Nakashita A, Wang Y, Lu S, Shimada K, Tschida T (2022) Ecology and genetic structure of the invasive spotted lanternfly Lycorma delicatula in Japan where its distribution is slowly expanding. Sci Rep 12:1543
Paini DR, Worner SP, Cook DC, De Barro PJ, Thomas MB (2010) Threat of invasives from within national borders. Nat Comm 1:115
Paini DR, Sheppard AW, Cook DC, De Barro PJ, Worner SP, Thomas MB (2016) Global threat to agriculture from invasive species. Proc Nat Acad Sci 113:7575–7579
Park M, Kim K-S, Lee J-H (2013) Genetic structure of Lycorma delicatula (Hemiptera: Fulgoridae) populations in Korea: implication for invasion processes in heterogenous landscapes. Bull Entomol Res 103:414–424
Petit JN, Hoddle MS, Grandgirard J, Roderick GK, Davies N (2009) Successful spread of a biocontrol agent reveals a biosecurity failure: elucidating long distance invasion pathways for Gonatocerus ashmeadi in French Polynesia. BioControl 54:485–495
Popkin G (2020) Can ‘sentinel trees’ warn of devastating pests? Sci 367(6485):1417
Pyšek P, Hulme PE, Simberloff D, Bacher S, Blackburn TM, Carlton JT, Dawson W, Essl F, Foxcroft LC, Genovesi P, Jeschke JM, Kühn I, Liebhold AM, Mandrak NE, Meyerson LA, Pauchard A, Pergl J, Roy HE, Seebans H, van Kleunen M, Vilá M, Wingfield MJ, Richardson DM (2020) Scientists’ warning on invasive alien species. Biol Rev 95:1511–1534
Rathe AA, Pilkington LJ, Gurr GM, Hoddle MS, Daugherty MP, Constable FE, Luck JE, Powell KS, Fletcher MJ, Edwards OR (2012) Incursion preparedness: anticipating the arrival of an economically important plant pathogen Xylella fastidiosa Wells (Proteobacteria: Xanthomonadaceae) and the insect vector Homalodisca vitripennis (Germar) (Hemiptera: Cicadellidae) in Australia. Aust J Entomol 51:209–220
Rathe AA, Pilkington LJ, Hoddle MS, Spohr LJ, Daugherty MP, Gurr GM (2014) Feeding and development of the glassy-winged sharpshooter, Homalodisca vitripennis, on Australian native plant species and implications for Australia biosecurity. PLoS ONE 9(3):e90410
Rathe AA, Pilkington LJ, Hoddle MS, Spohr LJ, Daugherty MP, Gurr GM (2015) Invasion pathway risk analysis for the glassy-winged sharpshooter (Homalodisca vitripennis): survival and reproductive success following simulated air transportation. Biol Invasions 17:2963–2973
Reitz SR, Gao Y, Kirk WDJ, Hoddle MS, Leiss KA, Funderburk JE (2020) Invasion biology, ecology, and management of western flower thrips. Ann Rev Entomol 65:17–37
Ricciardi A, Lacarella JC, Aldridge DC, Blackburn TM, Carlton JT, Catford JA, Dick JTA, Hulme PE, Jescjke JM, Liebhold AM, Lockwood JL, MacIssac HJ, Meyerson LA, Pyšek P, Richardson DM, Ruiz GM, Simberloff D, Vilá M, Wardle DA (2021) Four priority areas to advance invasion science in the face of rapid environmental change. Environ Rev 29:119–141
Roques A, Fan J-T, Courtial B, Zhang Y-Z, Yart A, Auger-Rozenberg M-A, Denux O, Kenis M, Baker R, Sun J-H (2015) Planting sentinel European trees in eastern Asia as a novel method to identify potential insect pest invaders. PLoS ONE 10(5):e0120864
Rugman-Jones PF, Hoddle CD, Hoddle MS, Stouthamer R (2013) The lesser of two weevils: molecular-genetics of pest palm weevil populations confirm Rhynchophorus vulneratus (Panzer 1798) as a valid species distinct from R. ferrugineus (Olivier 1790), and reveal the global extent of both. PLoS ONE 8(10):e78379
Saunders TE, Avila GA, Holwell GI (2021) Pre-emptive host specificity testing of Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae) reveals high parasitism levels against the New Zealand alpine shield bug in laboratory no-choice tests. Austral Entomol 60:411–421
Seebans H, Blackburn TM, Dyer EE, Genovesi P, Hulme PE, Jeschke JM, Pagad S, Pyšek P, Winter M, Arianoutsou M, Bacher S, Blasius B, Brundu G, Capinha C, Celesti-Grapow L, Dawson W, Dullinger S, Fuentes N, Jäger H, Kartesz J, Kenis M, Kreft H, Kühn I, Lenzner B, Liebhold A, Mosena A, Moser D, Nishino M, Pearman D, Pergl J, Rabitsch W, Rojas-Sandoval J, Roques A, Rorke S, Rossinelli S, Roy HE, Scalera R, Schindler S, Štajerová K, Tokarska-Guzik B, van Kleunen M, Walker KM, Weigelt P, Yamanaka T, Essl F (2017) No saturation in the accumulation of alien species worldwide. Nat Commun 8:14435
Seebans H, Blackburn TM, Dyer EE, Genovesi P, Hulme PE, Jeschke JM, Pagad S, Pyšek P, van Kleunen M, Winter M, Ansong M, Arianoutsou M, Bacher S, Blasius B, Brockerhoff EG, Brundu G, Capinha C, Causton CE, Celesti-Grapow L, Dawson W, Dullinger S, Economo EP, Fuentes N, Guénard B, Jäger H, Kartesz J, Kenis M, Kühn I, Lenzner B, Liebhold AM, Mosena A, Moser D, Nentwig W, Nishino M, Pearman D, Pergl J, Rabitsch W, Rojas-Sandoval J, Roques A, Rorke S, Rossinelli S, Roy HE, Scalera R, Schindler S, Štajerová K, Tokarska-Guzik B, Walker K, Ward DF, Yamanaka T, Essl F (2018) Global rise in emerging alien species results from increased accessibility of new source pools. Proc Nat Acad Sci 115:E2265
Seo M, Kim JH, Seo BY, Park C, Choi BR, Kim KH, Ji CW, Cho JR (2019) Effect of temperature on reproduction and parasitism of the egg parasitoid, Anastatus orientalis (Hymenoptera: Euplemidae). J Asia-Pacific Entomol 22:1013–1018
Shermer M (2004) Miracle on probability street. Sci Am 291:32
Turner RM, Plank MJ, Brockerhoff EG, Pawson S, Leibhold A, James A (2020) Considering unseen arrivals in predictions of establishment risk based on border biosecurity interceptions. Ecol Appl 30:e02194
Turner RM, Brockerhoff EG, Bertelsmeier C, Blake RE, Caton B, James A, MacLeod A, Nahrung HF, Pawson SM, Plank MJ, Pureswaran DS, Seebens H, Yamanaka T, Liebhold AM (2021) Worldwide border interceptions provide a window into human-mediated global insect movement. Ecol Appl 31:e02412
Urban J (2019) Perspective: shedding light on spotted lanternfly impacts in the USA. Pest Manag Sci 76:10–17
Valentine RE, Nielsen AL, Wiman NG, Lee D-H, Fonseca DM (2017) Global invasion network of the brown marmorated stink bug, Halyomorpha Halys. Sci Rep 7:9866
van Driesche R, Hoddle M, Center T (2008) Control of pests and weeds by natural enemies: an introduction to biological control. Blackwell Publishing, Massachusetts
Wakie TT, Neven LG, Yee WL, Lu Z (2020) The establishment risk of Lycorma delicatula (Hemiptera: Fulgoridae) in the United States and globally. J Econ Entomol 113:306–314
Weber DC, Hajek AE, Hoelmer KA, Schaffner U, Mason PG, Stouthamer R, Talamas EJ, Buffington M, Hoddle MS, Haye T (2021) Unintentional biological control. In: Mason PG (ed) Biological control—global impacts, challenges and future directions of pest management. CSIRO Publishing, Victoria, pp 110–140
Wyckhuys KAG, Day MD, Furlong MJ, Hoddle MS, Sivapragasam A, Tran HD (2021) Biological control successes and failures: Indo-Pacific/Oriental region. In: Mason PG (ed) Biological control—global impacts, challenges and future directions of pest management. CSIRO Publishing, Victoria, pp 438–466
Yang X-M, Sun J-T, Xue X-F, Li J-B, Hong X-Y (2012) Invasion genetics of the western flower thrips in China: evidence for genetic bottleneck, hybridization, and bridgehead effect. PLoS ONE 7(4):e34567
Yanow T, Kriticos DJ, Ota N, Avila GA, Hoelmer KA, Caron V (2021) Modelling the potential geographic distribution of two Trissolcus species for the brown marmorated stink bug Halyomorpha Halys. Insects 12:491
The author thanks Mark Schwarzlander and Peter Mason for the opportunity to submit this article to the BioControl. Aspects of the proactive work reported on here have been supported, in part, by the California Avocado Commission, Citrus Research Board, California Department of Pesticide Regulations, CDFA’s Specialty Crops Program, and CDFA’s Office of Pesticide Consultation and Analysis. Two anonymous reviewers provided excellent feedback and suggestions that improved this article.
This study was funded by Citrus Research Board, California Department of Pesticide Regulations, CDFA Specialty Crops Program, CDFA Office of Pesticide Consultation and Analysis, California Avocado Commission.
Conflict of interest
The author declares that there are no conflicts of interest.
No informed consent was needed for the writing of this article.
Research involving human and animal participants
This article does not contain any studies with humans or vertebrate animal subjects.
Handling Editor: Peter Mason.
About this article
Cite this article
Hoddle, M.S. A new paradigm: proactive biological control of invasive insect pests. BioControl (2023). https://doi.org/10.1007/s10526-023-10206-5