Early Warning Systems as a Component of Integrated Pest Management to Prevent the Introduction of Exotic Pests

When introduced to novel habitats, invasive alien plant pests have the potential to reduce fitness or cause aesthetic damage to naïve plant hosts, or to cause widespread mortality in both native and cultivated plant populations. Once established, the cost of mitigation, eradication, and damage and losses from invasive alien plant pests often exceeds the cost of preventing introductions from occurring. National plant protection organizations (NPPOs) have therefore implemented trade restrictions and regulations to minimize the introduction of alien plant pest species. To be effective, NPPOs must stay informed about pest species that may pose a threat to natural or agricultural systems. Early warning systems such as PestLens, the European and Mediterranean Plant Protection Organization Reporting Service, and others collect relevant and current plant pest information and disseminate it to NPPOs, thereby facilitating informed regulatory decision-making. Herein, we describe the processes and goals of some of the existing plant pest early warning systems and how these systems may be used.

Invasive plant pests (i.e., insects, weeds, and pathogens) alter ecosystem processes, disrupt trophic interactions, threaten biodiversity, and ultimately burden ecological and economic systems on a global scale (Pimentel et al. 2005, Pejchar and Mooney 2009, Bradshaw et al. 2016, Mollot et al. 2017. When introduced to ecosystems that lack coevolved natural enemies and host plant defenses, invasive alien species can substantially reduce host plant fitness and cause widespread mortality, leading to significant ecological, cultural, and economic losses (Aukema et al. 2011, Bauer et al. 2015, Rigling and Prospero 2018. For example, the introductions of two invasive forest insects, Cydalima perspectalis and emerald ash borer (Agrilus planipennis), to Europe and North America, respectively, resulted in large-scale loss of their preferred host plants and major alteration in canopy composition in affected forests (Bauer et al. 2015, Plant et al. 2019. Similarly, the fungus Cryphonectria parasitica, the causal agent of chestnut blight, was first detected in the United States in 1904 and has all but eliminated American chestnut (Castanea dentata) trees from North American forests (Rigling and Prospero 2018).
Economic losses and control expenses for invasive plant pests come with high price tags. It is estimated that global losses associated with invasive insects, plants, and pathogens account for up to 1.4 trillion USD annually (Pimentel et al. 2001, Bradshaw et al. 2016. In Great Britain alone, annual losses from and control of exotic invasive species are estimated to cost 2.2 billion USD (Williams et al. 2010). In the United States, it is estimated that yearly crop yield losses from invasive insects, plant pathogens, and weeds total 13 billion, 21 billion, and 24 billion USD, respectively (Pimentel et al. 2005). Additional costs can be attributed to the use of pesticides, herbicides, and fungicides, as well as damage to forest and urban systems. Individual species can cause notable economic damage within naïve ecosystems. For example, Asian longhorn beetle (Anoplophora glabripennis) is considered one of the most expensive insects in the world, costing 3 billion USD between the United States and Europe (Bradshaw et al. 2016). Similarly, the fungus Fusarium oxysporum f. sp. cubense, causal agent of Panama disease of banana, has devastated banana plantations wherever it has been introduced (Ploetz 2005(Ploetz , 2015. Between 1940 and1960, the pathogen wiped out vast plantations of 'Gros Michel' bananas in Central America, necessitating re-planting with a resistant cultivar. Losses during that time are estimated to have been over 2.3 billion USD (Ploetz 2005).
Invasive species introductions are often associated with trade. It is estimated that 54 out of 125 taxa listed in the European Database of the Invasive Forest Pathogens were likely introduced through pathways associated with trade (Hulme 2009, Liebhold et al. 2012, Vettraino et al. 2017. Further, in the last 30 yr, most invasive forest pathogens have been introduced through the trade of ornamentals intended for planting (Santini et al. 2013). Other common pathways for introductions include entry as contaminants or stowaways in live plant material, shipping containers, packaging material, airline baggage, and ballast (Liebhold et al. 2006, Hulme 2009, Liebhold et al. 2012. Increasing international trade has created more pathways for invasive species and accelerated the rate at which introductions occur (Hulme 2009). As globalization intensifies, the worldwide economic and ecological burden of invasive species is expected to increase (Levine and D'Antonio 2003, Hulme 2009, Seebens et al. 2015, Early et al. 2016. To prevent invasive alien species introductions through ports of entry, many countries (United States, Canada, Australia, China, etc.) have enacted port inspection and quarantine protocols (CFIA 1990, Ministry of Commerce 1991, International Plant Protection Convention 2006, Dooley 2007, Burgos-Rodríguez and Burgiel 2020. The United States government has enacted several pieces of legislation to regulate the movement of pests into and within its borders (Burgos-Rodríguez and Burgiel 2020). For example, the Federal Noxious Weeds Act of 1974 was established to control the spread of noxious weeds and grant authority to the Secretary of Agriculture to designate plants as noxious weeds (7 CFR § 360 2011). The Plant Protection Act of 2000 allows the United States Department of Agriculture (USDA) to conduct port inspections, regulate imports of high-risk plants to the United States, and place high-risk pests into quarantine status (Marbuah et al. 2014). Similarly, the 1990 Plant Protection Act of Canada prohibits any plant pest or associated host plant from being imported to or transported within Canada (CFIA 1990).
Due to the sheer volume of global trade, it is helpful for port inspectors to target their efforts to riskier commodities and shipments (Marbuah et al. 2014). It is useful to know which pests are moving most frequently, and on what commodities, to give port inspectors advance notice and information about their identification and to prepare regulations on imports, if necessary. This is often accomplished through the creation of lists of priority nonnative species that pose a risk to agricultural, urban, or natural habitats, combined with information about the pests' host plants and current global distribution (Reaser et al. 2020). Due to the plethora of plant pests that exist globally and the evolving nature of species invasions, the national plant protection organizations (NPPOs) that produce priority pest lists often rely on early warning systems that collect and disseminate emergent plant pest information in order to efficiently maintain them (Petter et al. 2011, Meissner et al. 2015.
Several early warning systems currently address the need for dissemination of current information on emerging plant pests, and each uses a unique methodology to identify pests that may cause economic or ecological damage if introduced to new regions of the world. These include reports from the European and Mediterranean Plant Protection Organization (EPPO), the North American Plant Protection Organization, and PestLens, a cooperative agreement between USDA Animal and Plant Health Inspection Service-Plant Protection and Quarantine (USDA-APHIS-PPQ) and North Carolina State University (Brunel et al. 2010, Petter et al. 2011, Meissner et al. 2015, NAPPO 2020a, among others. The present synthesis aims to describe the processes and goals of some of the existing plant pest early warning systems and to elucidate beneficial outcomes in invasive species prevention resulting from plant pest early warning information.

An Overview of Early Warning Systems
Early warning systems provide up-to-date, accurate information on emerging plant pests that may be a threat to agriculture or natural resources if they become established in new countries ( Table 1). For that reason, the target audience of each early warning system differs and may be associated with NPPOs or regional plant protection organizations to focus on the needs of the stakeholder regions. Early warning systems also differ in methodology and information sources. The remainder of this section describes the goals and processes of some plant pest early warning systems.

PestLens
PestLens serves as an early warning system for USDA-APHIS-PPQ concerning plant pests and pathogens that may pose a threat to United States agriculture and natural resources. Each week, PestLens analysts monitor a list of over 300 scientific journals, NPPO reports, Google alerts, newspapers, e-mail lists concerning invasive species, and other plant-health-related websites. The analysts evaluate content from each of these sources for its relevance to PPQ, which is determined by several factors, including: whether the information is new to PPQ, whether the plant pest is of quarantine significance to the United States, the potential economic impact of the pest if it were introduced, the likelihood of a pathway for introduction, and the likelihood that action by PPQ may be needed to prevent its introduction. The scope of PestLens includes new host information, new distribution records, detection of a pest in a new country where it is not yet established, eradication of a pest from a country, descriptions of new species with pest potential, and other research that may be of regulatory interest (Meissner et al. 2015).
Once important pest news is identified by the analysts, they write a brief article that includes the new information about the pest as well as background information such as its previously known host range and distribution. These articles are archived on the PestLens website and they are compiled into a weekly e-mail notification that is sent to PPQ employees and thousands of other subscribers. The information is then used by PPQ to make regulatory decisions about affected plants and plant products, and these decisions are documented within the PestLens website (Meissner et al. 2015).

EPPO Alert List and EPPO Reporting Service
The European and Mediterranean Plant Protection Organization (EPPO) generates an EPPO Alert List, which is a list of plant pests and pathogens that may pose a risk to the 52 member countries of EPPO (Petter et al. 2011, Roy 2011. The pests on the EPPO Alert List are chosen by the EPPO Secretariat based on the scientific literature and on suggestions by the NPPOs of the EPPO member countries (Roy 2011). Factors that may warrant inclusion into the EPPO Alert List include: newly described pests, reports of spread to new geographical locations, and reports of major outbreaks in the EPPO region (EPPO 2020a). Each pest on the EPPO Alert List has a fact sheet which contains information, such as the known hosts and distribution, the type of damage, the mode of dissemination, and potential pathways for spread to new geographical locations (EPPO 2020a). Some pests included in the EPPO Alert List may be selected for a Pest Risk Analysis (Petter et al. 2011, EPPO 2020a. Once a Pest Risk Analysis is completed, the pest may be placed on the EPPO A1/A2 list of pests that are recommended for regulation as quarantine pests (Roy 2011, EPPO 2020a. Pests that are not selected for Pest Risk Analyses stay on the EPPO Alert List temporarily, typically about 3 yr, and then they are removed from the EPPO Alert List and archived to a list of previously listed pests (EPPO 2020a, c). This allows the NPPOs of the EPPO member countries to monitor the pests that are on the alert list and take any appropriate actions, while not having the alert list become too lengthy (EPPO 2020a).

The European and Mediterranean Plant Protection
Organization also produces the EPPO Reporting Service newsletter, which is a monthly bulletin that reports on phytosanitary events concerning pests that may threaten the EPPO region, including both quarantine pests and emerging pests (EPPO 2020b). The EPPO Reporting Service reports on new hosts, new geographical locations, new pests, and new identification and detection methods (EPPO 2020b). The EPPO Secretariat chooses articles for the EPPO Reporting Service based on reports in the scientific literature, as well as official reports from NPPOs in the EPPO region (EPPO 2020b).

North American Plant Protection Organization Phytosanitary Alert System
The North American Plant Protection Organization Phytosanitary Alert System is a web-based system that provides official pest reports from the NPPOs of Canada, the United States, and Mexico. The Phytosanitary Alert System also provides Emerging Pest Alerts, which are news items about plant pests and pathogens that are not established in this region. These news items are obtained from public sources, including scientific journals, newspapers, records from port-of-entry interceptions, and domestic plant pest surveys. These reports have generally not been confirmed with the corresponding NPPO. The official pest reports and the Emerging Pest Alerts are intended to provide early warning to member countries about pests of concern to the region (NAPPO 2020b).

ProMED
ProMED is an e-mail list that disseminates information pertaining to disease outbreaks that may affect human health, both directly, as in human pathogens or toxins, and indirectly, as in diseases of plants and animals that are important for agriculture (Carrion and Madoff 2017). Subscribers can choose different ProMED mailing lists based on their areas of interest and their geographic region (Yu andMadoff 2004, Carrion andMadoff 2017). ProMED differs from some of the other early warning systems both in its broader scope and also that it uses informal and nontraditional information sources to generate its reports, including local media, on-the-ground experts, and professional networks (Carrion and Madoff 2017). ProMED focuses on outbreaks in new geographic regions, newly described diseases, and diseases for which the causal agent is unknown (Yu and Madoff 2004). In contrast, early warning systems associated with NPPOs (such as EPPO Reporting Service, PestLens, and the North American Plant Protection Organization Phytosanitary Alert System) often do not report on diseases for which the causal agent has not been identified, since identification of the pathogen species is typically necessary from a regulatory standpoint.

International Plant Protection Convention Pest Reports
The International Plant Protection Convention is a plant health treaty signed by over 180 countries. Nation plant protection organizations of each member country submit official pest reports as needed concerning the occurrence, outbreak, spread, or eradication of organisms that are quarantine pests in that country or that are quarantine pests for neighboring countries and trading partners. These pest reports are posted on the International Plant Protection Convention website, enabling the NPPOs of other countries to respond with appropriate changes to phytosanitary requirements (International Plant Protection Convention 2006). Website-Access the publicly available web archive of plant pest news Subscription-Subscribe to receive an e-mail notification when there is a new official pest report The table indicates the name of each early warning system, the URL by which it can be accessed, the regions for which it covers events, the breadth of plant pests covered, and how to access the information.

International Plant Sentinel Network
The International Plant Sentinel Network is founded on the premise that historically, many devastating plant pests were either not known to science or not known to be pests in their native ranges. Once these pests were introduced to new geographical regions, they caused severe damage to plants that did not co-evolve with them (Rigling and Prospero 2018). For example, the fungus Hymenoscyphus fraxineus is not known to be pathogenic in its native range but has caused widespread dieback of native European ash trees in Europe (Roy et al. 2017, Vettraino et al. 2017. The International Plant Sentinel Network identifies potentially destructive pests based on damage to plants cultivated outside their native range in arboreta and botanical gardens. Such findings may indicate that the pest or pathogen would be a serious threat if introduced to that plant's native range. The International Plant Sentinel Network is also used to identify pests that present a low risk so that resources can be re-allocated to more damaging pests. For example, based on host information obtained during a workshop at a botanical garden in California, the NPPO of the United Kingdom reduced the risk rating of goldspotted oak borer (Agrilus coxalis) and increased the risk rating of polyphagous shot hole borer (Euwallacea sp.) (Barham et al. 2016).

Discussion
Through their various methodologies for how information is gathered and prioritized for distribution, each early warning system has a slightly different and complementary niche. The International Plant Sentinel Network identifies potentially destructive pests based on damage to nonnative plants in arboreta and botanical gardens; ProMed identifies new pest events from informal and nontraditional sources, wherein the causal agent may not have yet been identified; PestLens reports primarily on scientific journal articles, but also NPPO reports, newspapers, e-mail lists concerning invasive species, and other plant-health-related websites; the EPPO Reporting Service newsletter focuses on reports in the scientific literature, as well as official reports from NPPOs in the EPPO region; and the North American Plant Protection Organization Phytosanitary Alert System provides official pest reports from the NPPOs of Canada, the United States, and Mexico.
Growers, scientists, and other stakeholders can access much of the information from early warning systems (Table 1), which keeps them informed of what threats may be coming. They can also report findings of new alien species to NPPOs (Suffert and Ward 2014). NPPOs and early warning systems then exchange information in both directions (Fig. 1). NPPOs communicate any new findings to regional plant protection organizations, such as EPPO and the North American Plant Protection Organization, whose associated early warning systems distribute alerts. Other early warning systems such as PestLens can amplify pest alerts by publishing notifications on the same events and distributing them to additional audiences. In return, early warning systems such as PestLens and the EPPO Reporting Service gather information on emerging pests from a broad range of sources and distribute this information to members of various NPPOs, who can then add species to a watch list or  other policy decisions. For example, the Emerging Risk System for Biosecurity in New Zealand uses alerts from early warning systems as inputs for their system, they are assessed, and risk analysis and regulatory changes are implemented as needed. Following a 2019 PestLens alert about the newly described apple chlorotic fruit spot viroid (ACFSVd) from Austria, the Emerging Risk System for Biosecurity in New Zealand conducted a risk assessment. Although the risk assessment concluded that the risk at that time was negligible, active monitoring ensued to collect additional information that could affect policy decisions (Biosecurity New Zealand 2020).
Early warning systems can also track a pest's movement between countries and document changes in host range over time. For example, the tobamovirus Tomato brown rugose fruit virus (ToBRFV) was described infecting tomato in Jordan in 2015 (Salem et al. 2016) and reported by PestLens in 2016. Affected plants exhibit leaf chlorosis and mosaic and unmarketable, wrinkled fruits with chlorotic spots (Oladokun et al. 2019, Yan et al. 2019. The North American Plant Protection Organization reported the first observation of ToBRFV outside of Jordan in 2018, when it was found in Mexico (NAPPO 2018) and the United States (Chitambar 2018, Ling et al. 2019. At the same time, PestLens shared a publication that reported the virus in Israel for the first time in 2017 (Luria et al. 2017) and also forwarded the Mexico finding from the North American Plant Protection Organization. In 2019, ToBRFV was found in tomato greenhouses in Germany (Menzel et al. 2019), and a spate of other detection and new location findings were observed and reported in 2019 in Europe, China, and Turkey (Fidan et al. 2019, Yan et al. 2019, EPPO 2020d. In 2020, the virus continued to spread and was reported elsewhere in Europe and in Egypt (Amer and Mahmoud 2020). It has now been found in Asia, Europe, the Middle East, and northern Africa (EPPO 2020d). It was found in the Netherlands in tomato seeds for planting from Peru (NVWA 2020), showing that the global seed trade is an effective means of dispersal of this virus. This finding was reported by EPPO and later by other early warning systems. In response to the rapid movement of the virus, trade restrictions have been enacted by numerous countries, including the United States (USDA-APHIS-PPQ 2019), Australia (DAWE 2020), and the European Union (EUR-Lex 2020). For example, on 15 November 2019, USDA APHIS issued a Federal Order imposing restrictions on imports of tomato and pepper seeds lots, transplants, and fruits from all countries where ToBRFV has been detected or reported (USDA-APHIS-PPQ 2019). Although the exact economic losses that were averted by introducing these restrictions are not known, ToBRFV spreads efficiently, causes between 30 and 70% yield reduction, and has the ability to cause major losses in the global tomato market, which is a multi-billion dollar industry (Globe Newswire 2019, WUSF 2019, Yan et al. 2019, FAO 2021.
By closely monitoring which pests are most frequently reported by early warning systems, from which countries, and what commodities tend to be infested, it may be possible to predict high-risk pests, commodities, or regions of origin (Pautasso et al. 2015, Steffen et al. 2015. Understanding likely plant pest invasion pathways and current inspection protocols is a critical first step to reduce the number of invasive alien species introduced through trade pathways. By collecting and disseminating relevant plant pest information, early warning systems play a crucial role in maintaining high priority pest lists that inform port inspection and quarantine regulations.

Conclusion
Increasing interconnectedness through trade requires constant vigilance on a global scale to limit the movement of plant pests across geopolitical boundaries. Early warning systems for plants pests are efficient systems that alert stakeholders, government authorities, and policy makers about contemporaneous high priority plant pest news. Several plant pest early warning systems (e.g., the EPPO Reporting Service, PestLens, and ProMED) currently operate to gather and disseminate pertinent information on plant pest developments from a variety of sources. Though the scope and methodology of these early warning systems differ, they have a common goal: to bring attention to high-risk pests before they are introduced to a new region so that targeted inspection efforts and policy decisions may be implemented as needed. Lastly, early warning systems act synergistically to document the global movement of plant pests and offer a valuable resource for identifying high-risk pests and commodities.