Integrating integrated pest management and sustainability into a biosecurity framework

2.1 Exclusion/prevention

Exclusion is always the first line of defense against invasion by pest species, as exclusion simply keeps the pest from entering and establishing. International policies related to exclusion of some pests of global significance are monitored by the World Health Organization (WHO) for human health (https://www.who.int/), World Organization for Animal Health (WOAH) for other animal health (https://www.woah.org/en/home/), and the International Plant Protection Convention (IPPC) for plant health (https://www.ippc.int/en/). To successfully prevent the entry or spread of a non-native species, every non-native species must be treated as invasive, unless there is adequate evidence to prove otherwise. It also is recommended that preventive measures must be taken at both the source and the destination of the invasion (McNeely et al. 2001). In the case of interdictions with regulatory significance, there must be cooperation between the different sectors such as trade, tourism, transport, and travel to develop new and innovative strategies and actions to address areas including awareness-raising, legislation, management, education, and training (McNeely et al. 2001). Oftentimes, exclusion is viewed more as a regulatory term rather than a term specific to IPM; however, preventing the arrival of a pest into a given management system is a logical component of IPM (Meyerson and Reaser 2002).

2.2 Early detection

Even with optimal border protection methods, it is not always easy or feasible to stop the entry of non-native species. In the case of insect pests, their small size, increased human travel and trade, and globalization often make exclusion or prevention difficult or non-feasible. Early detection is one of the most cost-effective and ecologically viable methods for controlling invasive species. It represents a critical second, domestic-level defense against the spread and establishment of invasive pest species. Furthermore, citizen scientists can be engaged in the early detection of these species. For example, in the United States, a member of the Plataspidae insect family, the black bean bug (Brachyplatys subaeneus (Westwood) (Hemiptera: Platasipidae)) recently was detected as established in Florida based on the observation and photograph of a citizen posting to iNaturalist (Eger et al. 2020). Extension programs and citizen science will be increasingly important for the early detection of non-native pests as the public becomes more aware of the economic and ecological impacts of invasive species (Crall et al. 2010; Pinkerton et al. 2019). Once a pest has been introduced into a new region, the success of any IPM program against such a pest will depend upon the correct and timely identification of the pest and the natural enemies associated with the pest. Therefore, agricultural producers, researchers, and extension specialists should embrace the rapid reporting and early detection of any pest that is new to an area. In fact, a detection that is early enough in the invasion process may be referred to as an isolated regulatory incident by regulatory personnel. Such a case occurred in the state of Florida a few years ago when a detection of the potentially invasive Old-World bollworm (Helicoverpa armigera (Hüber) (Lepidoptera: Noctuidae) was declared by the National Plant Protection Organization (NPPO) of the United States, the United States Department of Agriculture Animal and Plant Health Inspection Service Plant Protection and Quarantine (PPQ) program (USDA-APHIS-PPQ) as an isolated regulatory incident. Early detection results in significant cost-savings for agricultural producers and taxpayers. As another example, the occurrence of a small and isolated eradication program of the cottonseed bug, Oxycarenus hyalinipennis (A. Costa) (Hemiptera: Lygaeidae) in the Florida Keys by the local state regulatory agency, Florida Department of Agriculture and Consumer Services Division of Plant Industry (FDACS-DPI), protected over 12 million acres of cotton that are grown in the continental United States.

Expert identification of non-native, invasive species is often particularly difficult on a worldwide basis if diagnostic resources are unavailable within the country or region of an outbreak. In certain instances, invasive species also may represent a previously undescribed pest species. In addition to the descriptions of new species, uniform protocols for the molecular identification of species may not be available if the pest is a possible candidate for molecular diagnostics. For example, B. subaneus originally was misidentified with molecular methods as Brachyplatys vhalii (Fabricius) (Hemiptera: Platasipidae) in Panama (Aiello et al. 2016; Rédei 2016). In either case, the field survey specialists or IPM researchers need immediate access to designated expert laboratories to confirm specimen identity. They will need to seek expert specimen diagnosis any time an unusual pest outbreak occurs for a previously known organism. Some invasive species may superficially resemble native species, and the early detection of an established population assists with the implementation of a management program. Early detection can slow range expansion and avoid the need for costly long-term control efforts. In some cases, early detection of an isolated population also may result in the implementation of a formal eradication program.

2.3 Eradication, mitigation, and an official regulatory response

When exclusion fails and a non-native species is detected, there is a series of steps to consider, depending on the pest, in order to apply the appropriate potential response. Some general factors that are considered where applicable include:

1. Pest impact

2. Potential of the organism to be established

3. Host availability and distribution

4. Climatic conditions

5. Current distribution and rate of spread of the pest

6. Evaluation of all control tools/methods presently available, if any

7. Availability of any control tools that can be used to eliminate the population, or that can be used to reduce/control the population (FAO 2017).

Many non-native establishments pose little concern, and therefore illicit no response. If early detection has succeeded, the pest has a limited distribution, and appropriate tools are available, then eradication may be possible. If early detection has failed and the pest is widely distributed or has limited tools for its control, then eradication may be less feasible, and mitigation and regulatory measures are taken quickly to reduce impact and future spread of the pest (FAO 2017).

Eradication is often more related to regulatory programs and official government activities than to individual, homeowner, or farmer activities. Integrated pest management programs often begin during either the mitigation or response phase of an official government regulatory program. Eradication of invasive species is possible but is often costly. A good case study is recurring eradications of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), from Florida, which is native to Africa but was first detected in Florida in 1929 (Steck et al. 2019). The feasibility of eradication depends on the pest. Mediterranean fruit flies can be eradicated because there is an effective attractant, effective chemical control, and because sterile insect technique (SIT) has been well implemented. On the contrary, Caribbean fruit flies (Anastrepha suspensa (Loew) Diptera: Tephritidae) could not be successfully eradicated because the available attractant is less effective and the infestation was detected late. Florida spends an enormous amount of money surveying for several species of exotic fruit flies and on preventive SIT for C. capitata. This expense is justified because of the potential for agricultural damage. However, even with a reasonable bait and/or relatively early detection, eradication is not always possible. When an invasive species is determined to be established, academic researchers and extension specialists will shift to IPM strategies focused on the management of the pest and its impacts on the host or ecosystem.

4.1 Benefits of incorporating IPM into biosecurity

IPM is well understood within the context of invasive species management after a newly introduced pest is established. If eradication is initially the goal for an invasive species, the IPM plan may be vastly different due to the reactive nature of emergency and eradication programs which often precludes the implementation of a more long-term IPM program. In some instances, as discussed in more detail later for the emerald ash borer, Agrilus planippenis Fairmaire (Coleoptera: Buprestidae), a program begins as an eradication program and transitions to a long-term management program. Such necessary transitional programs demonstrate the need for improved ecological and pest scientific information before pest introduction, when possible, or immediately upon pest arrival and establishment.

Intentional and ongoing efforts for area-wide integrated pest management (AW-IPM) could facilitate improved local management for new pest introductions (Hendrichs et al. 2007). Improved trade, less restrictive country-to-country regulations, and fewer incidences of pests moving from one geographical region to the next could occur. Research has clearly indicated that AW-IPM is the most effective means for reducing pest damage, but unfortunately, many IPM programs remain operational more on a field-to-field basis due to the relational complexities of implementing AW-IPM. In many ways, AW-IPM is a modern perspective that relates to the historical concept of mutual cooperation between trading countries for the purpose of the prevention of pest movement and limiting quarantines and trade as much as possible for economic benefit (Devorshak 2012).

4.2 Challenges and considerations

Resources and public perceptions limit the incorporation of IPM into biosecurity. Resources may include human resources (persons to do the work), supplies, and field vehicles to travel to remote locations. AW-IPM can be particularly difficult if stakeholders do not understand the value of AW-IPM compared to IPM within an individual field. Stakeholders may include farmers who have a direct profit margin to consider, private industry, and the public. Depending upon the expected economic outcome of the product or the emotional or privacy concerns of a public citizen, AW-IPM requires consensus from everyone that the program is for the public good. Stakeholders of AW-IPM programs may also include government officials who need to understand the value and impact of AW-IPM for the public good. Communication care and concern may be similar for AW-IPM as for risk communication related to pest risk analysis (Neeley and Devorshak 2012). Specifically, AW-IPM relates to consensus and care communication as the stakeholders involved must understand the importance of participation.

5.1 Biological control

Classical biological control, or the importation of co-evolved natural enemies of invasive species to regulate the populations of the invader to below economically or ecologically significant thresholds, represents a key aspect of the response and long-term management of invasive species. When successful, classical biological control can provide long-term, low-cost, low-input control of invasive species (Duan et al. 2018). Below we provide summaries of relatively recent examples of the classical biological control of invasive species from both rapid response and long-term outlook perspectives.

5.2 A success story: Agrilus planipennis Fairmaire (Coleoptera: Buprestidae)

A. planipennis is an invasive species in the United States that attacks ash trees (Fraxinus spp.; Oleaceae). It was detected first in Michigan in 2002, and since then, has spread widely in the U.S. and Canada (Emerald Ash Borer Information Network 2023). Concern about this new invader was immediate given the cultural, economic, and ecological significance of Nearctic ash trees. Indigenous peoples consider ash to be of great cultural importance, featuring prominently in traditional basketmaking practices (Poland et al. 2017). Post-colonization, ash has been harvested for a variety of purposes because its wood is aesthetically desirable, strong, and flexible. Baseball bats, furniture, and tool handles all were commonly made from ash. Ash trees were also once popular as street and ornamental trees (Raupp et al. 2006). Ash trees provide food and habitat for other organisms and are critical in the healthy function of ecosystem services such as water and nutrient cycling (Kolka et al. 2018). Current management strategies, tree removal and insecticide injection, are costly and impossible to implement on a broad scale. The projected combined economic loss from A. planipennis in Illinois, Indiana, Michigan, and Wisconsin alone is estimated to be between USD $13.4 and $26 billion (Sydnor et al. 2011).

In response to the invasion of A. planipennis and the difficulty of its management, including the inefficacy of native natural enemies (e.g. Duan et al. 2014), classical biological control was selected as a management tactic. In large part, this was due to the fact that in its native range in Asia, A. planipennis is not a significant source of ash mortality, suggesting adequate regulation by co-evolved natural enemies (Liu et al. 2003, 2007]; Duan et al. 2012). As summarized in Bauer et al. (2015) and Duan et al. (2018), after extensive searching, three parasitoids were identified as candidate classical biological control agents for A. planipennis: Tetrastichus planipennisi Yang (Hymenoptera: Eulophidae), Oobius agrili Zhang and Huang (Hymenoptera: Encyrtidae), and Spathius agrili Yang (Hymenoptera: Braconidae). After extensive host range testing in which these parasitoids demonstrated strong preference for A. planipennis over native U.S. Agrilus and other coleopterans, the parasitoids were approved and released in Michigan in 2007 and were released subsequently in regions within the invaded range of A. planipennis (Bauer et al. 2015). While T. planipennisi and O. agrili established and spread after repeated releases, S. agrili did not (Abell et al. 2014, Duan et al. 2013, 2018]; Jennings et al. 2014). Given the threat of A. planipennis to ash trees and forests, additional biological control agents were sought. After additional foreign exploration and host range testing, Spathius galinae Belokobylskij and Strazanac (Hymenoptera: Braconidae) was approved for release. This species was thought to be a better phenological match for Nearctic conditions than S. agrili (Duan et al. 2018). Spathius  galinae has established and spread in the regions where it has been released (Butler et al. 2022; Quinn et al. 2022a). Continued evaluations of A. planipennis, parasitoid, and ash populations suggest that the introduced parasitoids have improved ash seedling survival while also increasing A. planipennis mortality (Duan et al. 2021). Further research is needed to determine the long-term impacts of the introduced parasitoids on A. planipennis-ash dynamics, but these recent findings are cause for cautious optimism.

One of the most important aspects of the response to invasion by A. planipennis has been cooperation and partnerships. Since the release of biocontrol agents of A. planipennis, their spread and establishment has been closely monitored. This was challenging given the number of locations and releases involved, as well as differences in the number of individuals of each species released at any given time, plus the number of agencies involved. To compile and share this information easily among A. planipennis researchers, mapBioControl.com was created. This database is maintained jointly by Michigan State University, the Midwest Invasive Species Information Network, USDA-APHIS, and USDA-FS (Forest Service). This database has allowed government and university researchers from institutions throughout the range of A. planipennis to locate and prioritize sampling and release areas. Another cooperative aspect of the effort to combat A. planipennis has been cooperative rearing efforts. With proper permits in-hand, government and academic labs alike coordinated, sharing rearing procedures, parasitoids, and A. planipennis larvae to support one another’s research efforts, sometimes between states. This cooperative approach also facilitated the initiation of multi-regional studies (Jennings et al. 2013; Quinn et al. 2022b). Studies such as these are critical, especially for invasive species like A. planipennis that disperse over long distances and infest natural areas.

5.3 Reframing failure: the case of Thrips palmi Karny (Thysanoptera: Thripidae) in Florida

There are very few cases of what the public might consider to be true “failures” (i.e., there are unexpected, overwhelmingly negative consequences) of classical biological control of invasive insects from the recent past. Instead of searching for dramatic, catastrophic failures, it is more relevant and productive to examine programs that resulted in little to no effect on the target organism’s population dynamics or damage. When considering such failures, it is important to bear in mind that classical biological control programs can take years, if not decades, before the true impact of the introduced natural enemy becomes apparent. It is important to delay judgement until a sufficient amount of time has passed and data has been collected. Access to information on failed efforts is often limited by a lack of published, peer-reviewed literature describing such cases.

One instance of a failed effort can be found in the attempted classical biological control of melon thrips (T. palmi) via the introduction of the parasitoid Ceranisus menes (Walker) (Hymenoptera: Eulophidae) in Florida. Melon thrips are a relatively polyphagous species that not only causes direct feeding damage to melons, eggplants, beans, and other economically important crops (Seal 1994), but are also competent vectors of plant viruses in the genus Orthotospovirus (Topsoviridae), such as melon yellow spot orthotospovirus (Adachi-Fukunaga et al. 2020) and watermelon bud necrosis (Ghosh et al. 2021). Florida has consistently been among the top producers of cucurbits in the U.S. In 2023, squash production alone was valued at more than USD $44 million in Florida (NASS 2024). Given the economic threat of T. palmi, its detection in Florida in 1990 led to its management becoming the subject of intensive investigation (Cannon et al. 2007; Castineiras et al. 1996). Classical biological control as a management option was quickly pursued. While the role of generalist predators in the biological control of thrips is well-recognized, their parasitoids are often less well-understood and more difficult to obtain (van Lenteren and Loomans 1999). C.  menes, a solitary endoparasitoid of thrips larvae, was selected for evaluation as a candidate classical biological control agent for T. palmi in Florida. In the laboratory, T. palmi was a suitable host for C. menes under a range of environmental conditions, leading to the first releases of multiple strains of C. menes in south Florida in 1992 (Castineiras et al. 1996). For reasons unknown, the parasitoid did not establish in Florida. No peer-reviewed discussions of the potential causes of this failure can be found. T. palmi remains a serious pest today, often managed with a combination of insecticides and generalist natural enemies (Canon et al. 2007). C.  menes and other thrips parasitoids have continued to be studied in the years since the unsuccessful biological control program (e.g., Froud and Stevens 1997, Murai and Loomans 2001, Triapitsyn et al. 1995, 2005]), so perhaps in the future more suitable strains or species of thrips parasitoids will be identified for evaluation as classical biological control agents of T. palmi.

5.4 Challenges in the implementation of biological control

Classical biological control as a discipline faces many challenges. The first is that classical biological control requires time and money to get started. As demonstrated by the examples above it can take many years and much financial investment for candidate classical biological control agents to be located, evaluated in the laboratory, and released, let alone evaluated in the field post-release. Obtaining permits for importation of a candidate biological control agent for study in a quarantine laboratory alone can take up to 2 years, with permits for release of a candidate agent into the environment taking just as long if not longer. These delays are a sensible precaution, ensuring a full evaluation of the potential benefits and pitfalls of an introduction. In the interim however, the target invasive species may continue to spread and cause harm. Mistakes made in so-called biological control efforts from the relatively distant past still remain at the forefront of stakeholders’ minds (e.g., mongoose releases in Hawaii – Palacio 2012). To assuage this trepidation, researchers must take special care to engage with the public, educating them on modern methods of classical biological control that make it so safe and discerning compared to the haphazard attempts from over 100 years ago. Unsuccessful classical biological control programs should be discussed and published with equal if not greater frequency as successful programs to help inform future efforts, hopefully leading to a greater likelihood of success. Additionally, it is important to ensure that the partnerships established with foreign collaborators from the invasive species’ native range are mutually beneficial. Historically, in biological control and many other disciplines, collaborations with other nations, especially those in low-income countries, have been one-sided at best. It is critical for modern practitioners of classical biological control to ensure that their partnerships with foreign collaborators are mutually beneficial rather than exploitative. Authorship, data, access, and any resulting benefits from the research should be shared freely with all collaborators and their stakeholders, with acknowledgement of all team members’ contributions. Finally, there can be difficulty in integrating classical biological control agents at the field-level in an agricultural context due to the sensitivity of most biological control agents to pesticides, as well as their need for food sources and habitats outside of cultivated areas.