https://orcid.org/0000-0002-3877-4162
Abstract
Changes in grain trading between Russian Far Eastern ports and North America in the late 1980s and early 1990s led to introductions of Lymantria dispar asiatica (Vnukovskij), formerly called the Asian gypsy moth (AGM), and the recognition of a new pathway for its transport. Unlike the pathways commonly used and regulated for commodities and for packaging material containing pest organisms, this presented a unique pathway for AGM. Vessels departing from the Russia Far East transiting to ports on the west coast of the United States (US) and Canada (CA) were infested with life stages of AGM and related species. Upon arrival in North America, eggs oviposited on the surfaces of the ships and its cargo hatched with larvae ballooning to vegetation surrounding port areas leading to the potential establishment of AGM populations. A multi layered monitoring and inspection program was developed to mitigate this risk of introduction, initially for Russian Far Eastern ports, and eventually to include specified areas of other Asian countries. In this article, we summarize and review the integral parts of this mitigation program, which include: risk assessments, AGM monitoring in foreign and domestic ports, vessel cleaning and certification by a government Plant Protection Organization (PPO) or its proxy, AGM surveillance, and eradication of introduced AGM in ports and other areas within the United States and Canada. The uniqueness of this program is characterized by its complexity, which involves coordinated efforts of PPOs, the use of various inspection organizations, and the support of ocean transportation industries.
Lymantria dispar dispar, L. (Lepidoptera: Erebidae) formerly called the European gypsy moth (EGM), was introduced in 1869 in Medford, Massachusetts presumably from France (Doane and McManus 1981; Liebhold et al. 1989; Forbush and Fernald, 1896). Immature larval stages feed mostly on leaves of deciduous trees (McManus and Csóka 2007) and North American (NA) established populations consist of flightless females and flight enabled males. Lymantria dispar are univoltine and overwinter as diapausing eggs contained in hair covered egg masses. Until recently, it was thought that one species of L. dispar inhabited all of Europe and most of Asia. Within this area, however, it was known that the species displayed significant behavioral and host plant utilization differences (Baranchikov 1988). West of the Ural Mountains there is limited flight, however, East of the Ural Mountains female EGM and Lymantria dispar asiatica (Vnukovskij) formerly called Asian gypsy moth (AGM), actively fly and indeed in Japan, Korea, and portions of China and the Russian Far East they are active strong flyers. Within its current expansive range in Eurasia however, the flight capabilities of the moth are not clearly defined. Keena et al. (2001, 2007, 2008) in a series of laboratory studies investigated the female flight propensity and capability of several Eurasian strains of L. dispar and hybrids with the North American gypsy moth (NAGM) strain of L. dispar dispar.
Lymantria dispar dispar is a notorious hitchhiker and has been moved unintentionally numerous times by human activities. As stated earlier it has now been established in the United States for over 150 yr and although classified as L. dispar dispar we consider it in this paper as having a distinct DNA makeup and a separate strain (NAGM) from the European strain (EGM) (Wu 2020). How it’s artificial, human assisted movement, and potential breeding effect flight abilities of subpopulations has not been studied extensively. Also, it is not known how selection pressures have led to the retention or loss of female flight. Females of Lymantria obfuscata (Walker), a species that has reduced, almost vestigial wings, which occurs in India has completely lost its flight ability; yet this species hybridizes with the NAGM and produces fertile hybrid offspring and all backcrosses through F3 generations (Victor Mastro, unpublished data). Scientists and regulators knew of these differences but there were no obvious pathways for introduction of AGM, flight enabled female moth populations to enter the United States at least on host material (USDA Forest Service 1991).
Since its introduction into North America, NAGM has been the suppression or eradication target of numerous Federal and State programs. Initial attempts at eradication gave way in the early 20th century to ongoing efforts to minimize its damage and to slow the moth’s spread to areas south and west of its original introduction site (Weseloh 2003). Populations were and are transported unintentionally by humans to non-infested portions of the United States (US) and Canada (CA). These incipient populations are still aggressively eradicated when discovered using a system of pheromone-baited traps (Schwalbe 1981; Kearns and Tobin, 2020) for detection and delimitation, followed by insecticide treatments and behavior-based control measures (i.e., mating disruption). Its damage peaked in NA in 1981 with reportedly close to 13 million acres defoliated in the eastern United States (McManus and Csóka 2007). The highest yearly suppression cost occurred in 2008 with a combined Federal and state expenditure of more than 22.5 million dollars (USDA Forest Service Gypsy Moth Digest 2.0.03). It was ranked third by Bradshaw et al. (2016) as one of the most destructive introduced pests. Federal and State agencies in conjunction with universities invested heavily in research to manage populations, eradicate introduced populations in uninfested portions of the United States, and slow the spread along the leading edge of the generally infested area (Leuschner et al. 1996; Sharov et al. 1998; Tobin and Blackburn 2007).
One important outcome of this research and key in supporting these management efforts was the identification and synthesis of the moth’s pheromone, disparlure, cis-7, 8-epoxy-2-methyloctadecane (Bierl et al. 1970, Leonhardt et al. 1992) and the development of an effective trap for its use (Schwalbe 1981; Tobin and Blackburn 2007). Pheromone baited traps are used for detecting and delimiting new introductions of NAGM that have been transported by human activities to the western and southern US. A larger capacity trap, milk carton trap (Victor Mastro, unpublished data, Otis Laboratory Reports) is used for monitoring the spread along the leading edge of the generally infested area. Because pheromone traps capture male L. dispar moths, which are strong fliers (females of the North American strain are flightless), male captures accurately reflect the geographic distribution and to an extent the density of a population (Elkinton and Cardé 1981). Control measures for the subsequent generation can largely be based on the geographic distribution of male captures. Adult moths do not feed, and males live only a few days once they emerge from their pupal cases. Similarly, females are short lived and will usually mate and oviposit a single egg mass within a few days after emergence. If unmated they will eject unfertilized eggs within a few days and perish.
We refer to L. dispar dispar, (L.) the North American populations with females that do not fly as ‘NAGM’ because of their European origin. However, for regulatory purposes, AGM not only includes L. dispar asiatica (Vnukovskij) but also L. dispar japonica (Motschulsky) and three other very closely related species L. umbrosa, (Walker), L. albescens (Hori & Umeno) and L. postalba (Inoue), although L. postalba could be relegated to synonymy under L. albescens (Djoumad et al. 2020). Female AGM are reportedly strong fliers and gravid females may migrate over long distances (Baranchikov 1988). This behavioral characteristic, female flight, would render management strategies employed in North America, based on male captures in pheromone-baited traps, less effective because the next generation’s geographic distribution may not be defined by the pattern of male captures. Treatment boundaries therefore cannot be based on the limited natural movement of immature gypsy moth life stages (Tobin et al. 2004).
Ballooning by neonates, a second mechanism for dispersal, is thought to result in relatively short distance movement under most circumstances (Mason and McManus 1981). Lymantria dispar subspecies of Asian origins are also known to have a broader host range than EGM. A large host range covering over 100 botanical families would enhance the probability of AGM establishing in a new environment and increase the potential for damage (USDA APHIS PPQ 2014). Tkacz (l991) estimated the economic impacts of the introduction of AGM on Siberian logs and found significant impacts on US softwood production and utilization. Later Prestemon et al. (2006) evaluated the economic impacts of introducing the AGM and the nun moth, Lymantria monacha (L.) on Siberian softwood logs under four different regulatory regimes. This study predicts high loses to the US forest product sector over the 28-year period used in the model. These losses did not include ecological or non-timber values which have been shown to be far greater than timber loss for damage caused by NAGM in the Eastern United States (Leuschner W.A. 1991; Leuschner et al. 1996).
It was in this setting and level of knowledge that reports of the port introductions of AGM in British Columbia, CA and Washington and Oregon US in the early 1990s gained significance (Savotikov et al. 1995). Russia had begun importing large quantities of CA and US grain, primarily wheat. Vancouver (BC), Vancouver (WA), Tacoma (WA), and Portland (OR) were the major ports loading grain into ships transiting from the Russian Far Eastern ports, mainly Nakhodka, Vostochny, and Vladivostok. The first report of an AGM introduction was by Canadian Agricultural Inspectors in 1991 who found dispersing neonates on their clothes when boarding Russian grain hauling ships in Vancouver (BC). Later, it was discovered that some of the neonates were carried by onshore winds up and over grain silos to vegetation in and near the port area where adult males were later captured.
The Russian ports where these grain ships originated are located at the southern tip of the Primorsky Krai in an area comprised of low mountains, vegetated primarily with Mongolian oak, Quercus mongolica (Fisch. ex Ledeb.). This oak and other tree species found in this area are preferred hosts for AGM populations (Ilyinykh et al. 2013). Suitable conditions (i.e., favorable weather, low levels of disease such as the nucleopolyhedrosis virus (NPV), and low parasite/predator populations) contribute to AGM population outbreaks (Lee et al. 2010, Alalouni et al. 2013). The outbreak populations are cyclic but are not predictable for either magnitude, location, or periodicity.
Dispersing adults from outbreak populations are attracted to bright light sources (Wallner et al. 1995). Lighting at the Russian ports and ships at anchorage are attractive sources of light and ports are located very close to vegetated hills and low mountains. Gravid females dispersing to ports lay egg masses around light sources on ships and on other lighted substrates in the port area (Fig. 1). Individual egg masses usually consist of 600–1000 eggs but may have as many as 1400. AGM populations surrounding these three Russian ports during the late 1980s and early 1990s were so high, that Russian port personnel reported ship decks had to be cleaned of expired AGM adults with shovels (V.C. Mastro personal communication). Suddenly, this non-apparent pathway, where no host material is involved in transport, became an obvious source of introduction. Later, USDA APHIS (Animal and Plant Health Inspection Service) and State agricultural inspectors from WA and OR Departments of Agriculture found egg masses on ships transiting from Russian ports. Trapped adult males from areas near Tacoma, WA, and Portland, OR were found to be Asian genotypes (Gibbons 1992).
Asian gypsy moth adults in the port area of Olga, Primorsky Krai, Russia (2013).
Lymantria dispar pheromone traps are annually placed throughout non-infested portions of the southern, central, and western US to detect introductions of eastern NAGM and AGM. In the United States, the L. dispar management strategy is based on cooperative pheromone trap surveys to detect introductions early, sometimes in the same year of introduction, enabling eradication of populations soon after introduction when populations are small and confined to a restricted geographic area (Hajek and Tobin 2009). Trapping surveys have been modified since 1991 to include port areas where AGM introductions may occur.
To address this mode of introduction, hitchhiking on ships, and the regulatory status of the Asian strains of L. dispar, APHIS Plant Protection and Quarantine (PPQ) convened a meeting of USDA scientists, regulators, and Canadian officials in Washington, DC. Meeting topics included how to address this new pathway and, more importantly, how to categorize L. dispar of Asian origin, which were then considered to be in the same taxon as the population that was well established in the eastern United States and Canada. Outcomes of this meeting were to: 1) treat these Asian populations for regulatory purposes as a separate species; 2) develop an effective management strategy for excluding introductions of Asian varieties; 3) develop a survey strategy to detect introductions and, 4) develop an eradication plan to address any introductions that did occur.
The uncertainty about the relationships in the Lymantria group was explored by Goldschmidt (1934) and Schintlmeister (2004). It was not until Pogue and Schaefer (2007) partially clarified the taxonomy of this complex that some taxonomic questions were resolved. Pogue and Schaefer (2007) separated the Asian strains of L. dispar into three subspecies: Lymantria dispar dispar, L. dispar japonica and L. dispar asiatica. In 2010 (deWaard et al. 2010) expanded a barcoding reference library of the Lymantria species which further clarified some taxonomic questions. Recent work has further added to the knowledge (Wu et al. 2015) of genetic differences between and within these three subspecies and the related species, L. umbrosa. Newly refined molecular procedures can also determine to a more precise scale of the point of origin of intercepted AGM. These methods are currently used when specimens are found on ships or cargo. Because ships may visit several Asian ports before transiting to a North American port, this ‘point of origin identification’ can help direct program personnel to enhance inspection procedures on ships where the life stages originated. Using the same identification methodology trapped males can also be used to indicate point of origin and where additional US and CA exclusion resources need to be directed.
Currently, a nuclear marker FS1 (Pfeifer et al. 1995) and a mitochondrial marker (Bogdanowicz et al. 1993, 2000) are used to categorize males captured in traps or other life stages intercepted on ships or cargo. If these two markers provide inconclusive results further analysis is conducted using microsatellites (Bogdanowicz 1997; USDA 2019), and mtDNA sequences (Wu et al. 2020). Also, all males captured in traps outside of port areas, in areas free of NAGM, are tested. In the eastern US, where NAGM is established, captured males are subsampled to screen for possible introductions of AGM genes in the North American population.
Initiations of the Russian Far East Port Monitoring Program
Russian and US Regulatory and Forestry officials and scientists met in the Russian Far East in 1992 to discuss ship infestations and determine whether measures could be undertaken at the points of origin to mitigate the problem. Russian forestry’s official opinion was that defoliating populations presented little to no adverse effects to property and recreation values, or economic impacts to industry. The effects on an oak dominated forest were negligible because Q. mongolica had little commercial value. However, Russian Forestry and Quarantine officials were sympathetic to the US and CA problem. Moreover, the costs of ships being delayed or denied entry into NA ports would be costly for shipping companies. Although these early efforts focused on the exchange of information, some preliminary monitoring for AGM was initiated. It was not until 1993 that an official AGM port monitoring program began in the Russian Far East.
Through this established program, we discovered that population densities were uneven in forested areas and when outbreaks occurred defoliation was often spotty. Although populations are cyclic, cycles are neither regular nor predictable. The source of AGM adults congregating in port areas was and to some extent remains unknown. It likely varies annually depending on the location of outbreak populations and the climatic condition when adults emerge and take flight. Early reports suggest that even female adults in some Russian regions can fly as far as 100 km or cross mountain ranges (Rozkhov and Vasilyeva 1982; Baranchikov 1988). However, it is likely that most adults arriving in port areas are local in origin.
We established a cooperative two-pronged approach to monitor AGM activity in forested areas surrounding ports and within ports. Monitoring tools were adopted based on the utility of the data they would generate and the practicality of employing them. In regulatory programs for pests this AGM monitoring effort may be unique in terms of its extent, methodology, and due to monitoring activities conducted within vegetation that is not a commodity and will not be moved in trade.
Monitoring AGM Populations in Russia
A Cooperative Agreement was signed in 1993 between USDA APHIS, USDA Forest Service, Russian Federal Forestry Agency (RFFA), and the All Russian Plant Quarantine Center (ARPQC) of the Federal Service for Veterinary and Phytosanitary Surveillance of the Russian Federation (FSVPSRF). This program was designed to alert US and CA officials to AGM population increases in and adjacent to ports and employ ship inspection procedures for vessels transiting to North American destinations. The program was conceived to mitigate accidental transport of AGM by this newly discovered pathway. Elements of this strategy include: 1) a grid of AGM pheromone-baited ((+)-disparlure) traps extending 20 kilometers from the three Russian ports into adjacent forested areas, 2) installing a grid of AGM pheromone-baited traps within the port boundaries, 3) strategically placing light traps within the ports to monitor adult AGM presence and abundance, and 4) establishing AGM female oviposition monitoring stations (1 m2) on vertical surfaces within the ports. Oviposit monitoring locations were selected based on a history of AGM female attraction as evidenced by an abundance of old egg masses surrounding a port lighting source.
Forested Areas
In forest areas extending 20 km from the port boundary, (+) disparlure baited high capacity ‘milk carton’ traps were placed along roads and hiking/walking paths to facilitate weekly trap collections. The data collected provided a yearly account of population densities and AGM population trends over time. We also explored sampling and monitoring other life stages, egg masses, and larval densities. We determined this was not practical and did not provide an accurate picture of adult densities, the critical stage for ship/cargo contamination. Two additional species, the rosy gypsy moth, L. mathura (Moore), and the nun moth, L. monacha (L.), which have been found to use this unique ship pathway were also included in Russia’s monitoring program in 1999 and 1994, respectively. Traps baited with (+) disparlure were also checked for the presence of L. monacha males that are of regulatory concern. Lymantria monacha males also respond to (+) disparlure, the singular active component in L. dispar pheromone dispensers, although a three-component blend, monachalure, would be more attractive to the males (Gries et al. 1997). Additional traps with a specific lure for L. mathura (Oliver et al. 1999, Gries et al. 1999) were also installed when the attractants became available. This species, another Asian defoliator that reaches outbreak populations in Asia including the Russian Far East, has been intercepted on ships originating from Russia Far Eastern ports. In addition, L. mathura egg masses are more difficult to locate on ships or cargo because females usually oviposit several small egg masses in cracks and crevices whereas AGM females usually oviposit a single buff colored egg mass on the surface of objects.
Port Areas
In the port areas, pheromone baited traps are also deployed to provide a measure of adult male presence and abundance. Although the numbers of males in traps are not a direct measure of female density it provides a daily indication of the overall number of adults in the port environs. Light traps and oviposition monitoring stations provide more direct measures of flight for female AGM and other target species in the ports; however, both tools have limitations. Ports are brightly lighted at night; thus, port lighting competes directly with light traps. Locations for light traps are also limited by available power sources and the security, safety, and accessibility of the location. Monitoring oviposition sites are located on light colored building walls that have an accompanying light fixture. Weathering of the walls painted surfaces, condition of the light fixture, and other temporary or permanent changes in the port environs all have an impact on how these sites perform.
Originally, only four port areas were included in the surveys: Vladivostok & Russky Island, Nakhodka, and Vostochny. Russky Island is not a commercial port, but it resides in the center of the bay where Vladivostok’s commercial port is located. Abundant host vegetation occurs on the island and it is thus included in the monitoring program. These four areas are designated ‘Level I’ or primary ports due to the volume of ship traffic transiting to NA or other overseas locations that require a phytosanitary ship inspection certificate including NA ports. Nakhodka and Vostochny occupy opposite sides of another large bay about 80 km east of Vladivostok. It became apparent that other smaller ports in Russia also harbored AGM populations, and that ship infestations did occur at these smaller ports before entering and transiting from the Level I ports.
Accordingly, an additional nine ports were added to the AGM monitoring program including: Olga, Vanino, Slavyanka, Zarubino, Plastun, Pos’et, Kozmino, Korsakov, and Kholmsk. These additional ports are designated ‘Level II’ ports and are only monitored with pheromone traps. Weekly pheromone trap catches of adult males within the forest area and ports were used to establish the period of risk for ship infestation. High risk periods were determined by adult moth flight. Overall, the high-risk period for all three species of lymantriids in the Russian Far East occurs from July through September.
Ship Inspection Procedures for AGM
A pre-departure ship inspection program was initiated in Russia in 1994. Ships scheduled to transit to North American ports are inspected by Russian Plant Quarantine personnel and if necessary, cleaned of egg masses and other life stages before leaving Russian ports. The Russian Quarantine Service attempts to inspect ships just before departure to US and Canadian ports at the ships last port of call in the Russian Far East. Inspected ships are issued a certificate of compliance, which allows them to enter NA ports where they can be further inspected by US and Canadian officials. At US ports, in the absence of a certificate of compliance, a ship can be held and inspected offshore with the assistance of the US Coast Guard. To track and identify high risk ships for entry into NA ports, US and CA program personnel developed a high-risk period for each monitored port using expected egg hatch periods for the ports of entry and AGM adult flight periodicity data for the ports of origin. If a ship is found with AGM life stages, either during a NA port inspection or an offshore inspection, further cleaning protocols are initiated. Failure of a second inspection may result in refusal of docking rights.
Ships may stop at several ports in Asia that are possible sources for AGM contamination, so it is the responsibility of the shipping line to ensure that an inspection occurs at the last Asian port of call. This was a problem before other AGM host countries began a vessel certification program which is described in more detail below.
The monitoring program provides data that indicates where populations are increasing around Russian ports. This also provides an early warning to North American regulatory inspection and monitoring officials since infested ships would not be high risk until the following spring when eggs have experienced satisfactory cold to meet their required diapause period for hatching. Ships present in the Russia ports during the egg laying period are designated high priority for ship inspection in NA ports. A critical time for successful AGM introduction will occur when eggs have met the diapause requirements, when weather conditions at the port of entry are favorable for egg hatch, and surrounding port vegetation is suitable for larval establishment and survival.
The shipping industry supports and finances vessel inspections in countries where AGM is endemic. Information generated by the program is shared between cooperating countries including others that may be at risk (New Zealand, Australia, and Chile). At risk countries may also require phytosanitary inspection certificates if a ship has visited a country where AGM is endemic. Other countries that have since been identified as an AGM source have been added to the monitoring and exclusion effort. These include Japan, South Korea, and China. These three source countries vary in respect to their versions of a monitoring/inspection program and differ in the data generated and shared. Results of this program highlight a holistic approach and other possible applications to exclude exotic introductions which are discussed below.
Added Port Mitigation Measures
Other mitigation procedures included reductions in port lighting and ship lighting at anchorage. This included encouraging ship loading during daylight hours when AGM females would not be attracted to ship or port lights (Wallner et al. 1995). Shipping companies are alerted to AGM presence in the ports and provided with information on AGM life stage descriptions and probable locations on ships where egg masses are likely to be found. Ship inspectors are alerted during high risk periods when the port monitoring tools begin to detect adults in the port area or in surrounding environs.
Additional Points of Origin
When US, CA, and Russian inspectors started to intercept egg masses on ships transiting from other foreign ports it became apparent that other countries should be included in the AGM pest exclusion program. Ports in Japan, South Korea, and China were assessed for AGM risk by USDA and Canadian regulators and scientists. Similar to Russia, pheromone-bated traps were deployed in each country, weekly trap catch data was used to establish the periods of high-risk. These high-risk periods vary by country and latitude but generally, it is a two-month period for each port area. Factors included in the analysis were: AGM presence and previous histories of outbreak populations, the presence of favorable AGM habitats near port areas, and interceptions of egg masses on ships in NA ports presumptively originating from these overseas ports. Concurrently, representatives from the USDA’s APHIS and the Forest Service met with representatives from the respective agencies of the three countries to discuss how a port monitoring and ship inspection program could be initiated and conducted within each country. There were considerable obstacles associated with negotiating these agreements. In the case of South Korea, changing a federal law was required to permit ship inspections.
Currently, there are AGM programs functioning in all three countries. Table 1 provides a list of the organizations responsible for ship inspections in the four countries. In Russia, it is the government regulatory organization while in the three other countries, they are private organization(s) under the direction of the appropriate government agency: The General Administration of Customs of the Peoples Republic of China (GACC) for China; Animal, and Plant Quarantine Agency (APQA) for South Korea, and the Ministry of Agriculture, Forestry and Fisheries (MAFF) for Japan. In 2009, the activities reported in this paper resulted in the North Atlantic Plant Protection Organization (NAPPO) adopting RSPM 33 which covers guidelines for the movement of ships and cargo from AGM infested areas.
Approved AGM vessel inspection agencies and companies for Russia, China, Japan, and Korea
| Russia (Far East Ports) | Federal Service for Veterinary and Phytosanitary Surveillance of the Russian Federation |
| South Korea (all ports) | International Plant Quarantine Accreditation Board (IPAB) |
| China (all ports on or north of 31°15′N) | China Certification and Inspection Group, LTD |
| Japan (all ports) | All Nippon Checkers Corporation (ANCC) |
| Japan Cargo Tally Corporation (JCTC) | |
| Nippon Kaiji Kentei Kyokai (NKKK) | |
| Shin Nihon Kentei Kyokai (SNKK) | |
| Nineteen additional certification companies |
| Russia (Far East Ports) | Federal Service for Veterinary and Phytosanitary Surveillance of the Russian Federation |
| South Korea (all ports) | International Plant Quarantine Accreditation Board (IPAB) |
| China (all ports on or north of 31°15′N) | China Certification and Inspection Group, LTD |
| Japan (all ports) | All Nippon Checkers Corporation (ANCC) |
| Japan Cargo Tally Corporation (JCTC) | |
| Nippon Kaiji Kentei Kyokai (NKKK) | |
| Shin Nihon Kentei Kyokai (SNKK) | |
| Nineteen additional certification companies |
Approved AGM vessel inspection agencies and companies for Russia, China, Japan, and Korea
| Russia (Far East Ports) | Federal Service for Veterinary and Phytosanitary Surveillance of the Russian Federation |
| South Korea (all ports) | International Plant Quarantine Accreditation Board (IPAB) |
| China (all ports on or north of 31°15′N) | China Certification and Inspection Group, LTD |
| Japan (all ports) | All Nippon Checkers Corporation (ANCC) |
| Japan Cargo Tally Corporation (JCTC) | |
| Nippon Kaiji Kentei Kyokai (NKKK) | |
| Shin Nihon Kentei Kyokai (SNKK) | |
| Nineteen additional certification companies |
| Russia (Far East Ports) | Federal Service for Veterinary and Phytosanitary Surveillance of the Russian Federation |
| South Korea (all ports) | International Plant Quarantine Accreditation Board (IPAB) |
| China (all ports on or north of 31°15′N) | China Certification and Inspection Group, LTD |
| Japan (all ports) | All Nippon Checkers Corporation (ANCC) |
| Japan Cargo Tally Corporation (JCTC) | |
| Nippon Kaiji Kentei Kyokai (NKKK) | |
| Shin Nihon Kentei Kyokai (SNKK) | |
| Nineteen additional certification companies |
Japan utilizes 23 third party private companies to conduct ship inspections and issue certifications. The private companies’ personnel training and oversight is provided by MAFF. Pheromone baited traps were also initially placed in 53 Japanese port areas to provide data on population trends and establish a high-risk period for each port. Trapping data was shared with the US and CA through 2009 when trapping was discontinued because of workforce constraints. On Japan’s northern island of Hokkaido, there is a unique situation where a closely related species, L. umbrosa, is endemic. This species occupies a portion of the island in addition to L. dispar japonica which also occurs on the island. These species hybridize but only produce sterile offspring (Higashiura et. al. 2011. Both species respond to (+) disparlure baited traps. L. umbrosa has been captured in a pheromone trap in the United States.
The AGM ship inspection program officially began in South Korea in 2010. It is similar to the program in Japan, but only the International Plant Quarantine Accreditation Board is conducting ship inspections and issuing certificates (Table 1). Certificates state that the ship is free from AGM life stages and this information is shared with US and CA regulators upon arrival in a North American port. Pheromone baited traps were placed in 8 major ports in 2008 and 11 ports in 2009, these were supplemented by light traps in a few select ports before 2012. Thirty-three ports are currently monitored with pheromone baited traps, and data is shared with North American cooperators.
A similar vessel AGM inspection program was initiated in 2011 in China. China’s certification and inspection Group LTD (CCIC) conducts vessel inspections under the supervision of the General Administration of Customs of the People’s Republic of China (GACC), formerly the General Administration of Quality Supervision, Inspection, and Quarantine of the People’s Republic of China (AQSIQ). In China, port trapping was organized by the Chinese Academy of Inspection and Quarantine (CAIQ) and traps were placed in major port areas. For example, CAIQ reported that traps were placed in 58 ports in 2015. Both CAIQ and CCIC conveyed results to the North American regulatory agencies during US-Canada-China meetings on AGM. Historically, Australia, New Zealand, and Chile share and use the information generated in port areas of the four AGM high risk countries.
Results of AGM Adult Trapping
Based on male moth trapping as a measure of adult population densities, AGM populations vary widely from year to year and from location to location (Fig. 2). Within Russia, the trap captures on Vladivostok and Russky Island, which are only a few kilometers apart, appear to indicate similar population increases in 2006, 2007, 2014, but were dissimilar in 1996 when there were large increases in male captures on Russky Island but not within the port area of Vladivostok. There is some synchrony among AGM populations in the Level I ports (Fig. 3). Trapping results in Russian Level II ports revealed that some of the ports may be large contributors to ship infestations. Olga, Plastun, and Korsakov all over time have had high trap catches. Because only traps are used for monitoring populations in Level II port areas, we assume the captures are reflective of AGM populations in the surrounding forests due to the lack of vegetation within the ports
AGM mean male moth trap captures per trap per year in Russian Far East Ports.
Russian Level I ports AGM mean male moth trap captures per trap per year.
Generally, the number of male moths captured in Russian Far East ports were much higher than those in South Korean ports for all years except 2019 (Fig. 4). When male AGM captures were compared between Russia and Japan from 2005 to 2009, the mean number of male moths captured per trap per season was higher in Japan than in Russia for 3 of the 5 yr (Fig. 5). There does not seem to be a significant correlation between yearly trap captures of male AGM moths between all four countries.
Mean number of AGM males captured per trap per year in port areas of Korea and Russia from 2008 to 2019.
Mean number of AGM males captured per trap per year in port areas of Japan (11 ports) and Russia (10 ports) from 2005 to 2009.
Ship Inspection Results
Vessel inspections started in various years; Russia (1994), Japan (2007), South Korea (2010), and China (2011). The number of inspected vessels with AGM certificates berthing at US ports has increased significantly but varies from year to year (Fig. 6). The percent of visiting vessels with AGM certificates originating from AGM host countries averages approximately 85% for the US and 97% for Canadian ports (Fig. 7). The actual percentage with certificates entering US ports might be higher but they simply were not reported to US inspectors. The US tracks the global AGM vessel environment, targeting high risk AGM vessels arriving at the US for inspection. However, a ship that arrives from a host AGM country following the removal of a large number of life stages, will be targeted for inspection upon arrival in the US.
Number of vessels inspected at ports in the US and Canada from 2012 to 2019.
Percentage of vessels with phytosanitary certificates berthing at ports in the US and Canada from 2012 to 2019.
According to the Canadian Food Inspection Agency (CFIA), Canada inspects on average approximately 30% of vessels arriving from host AGM countries. A total of 170 vessels were found infested out of 3,839 inspected from 2012 to 2019. In 2019, 98% of vessels arriving in Canadian ports had AGM free certificates, which is an increase from 2012 when this percentage was 87% (CFIA 2020).
Summary
The global shipping network is widely recognized as a pathway for invasive species introductions (Fig. 8). Since 1993 when Russia started inspections 12,350 ships have been certified free of AGM. The number of vessels found contaminated by AGM fluctuated annually depending on the population levels in host port areas. Although monitoring and ship inspections overseas have significantly reduced the risk of introductions, AGM introductions still occur. These may be the result of failures in the ship inspection programs or it may be that AGM is using other pathways to enter North America. The inspection agencies know from experience that AGM life stages including egg masses, pupae, and newly emerged live adults have been found on shipping containers and other shipped objects including commercial shipments of pipe, metals, munitions, and vehicles. In the US, introductions of AGM have been discovered on 62 occasions between 1991 and 2019 (Table 2). Based on data (CERIS 2019, 2020) provided by US Cooperative Agricultural Pest Survey (CAPS) program and subsequent data analysis, several eradication projects were initiated. Even when an introduction is discovered early, before spreading, an eradication program can result in expensive treatments. In 2016, the state of Oregon estimated $2.1 million was spent on an AGM eradication (Williams 2016), and the requested budget for AGM eradication in 2016–2017 in the state of Washington was $4,852,000 (Carlen 2016). Eradication programs for L. dispar introductions in Oregon over the previous 40 yr cost approximately $60 million (Kearns and Tobin 2020).
Detections of AGM in different states of the continental US using disparlure baited traps through CAPS program (EM: Egg mass) *Lymantria umbrosa
| US State | County | Detection year (number of cases) | Subtotal |
|---|---|---|---|
| WA | Snohomish | 1994 (1), 2018 (1), 2019(1*) | 3 |
| WA | Kitsap | 1994 (1), 2018 (1) | 2 |
| WA | King | 1991(5), 1995(2), 1996(1), 1997(1), 1999(1, 1 EM**), 2015(2), 2016(1 EM) | 13 |
| WA | Pierce | 1991 (4), 1993 (1), 1994 (6), 1995 (2), 1997(1), 2015(4) | 18 |
| WA | Thurston | 1995 (1), 2015 (2) | 3 |
| WA | Clark | 2015 (1) | 1 |
| OR | Columbia | 2006 (1) | 1 |
| OR | Multnomah | 1991 (1), 2000(1), 2005 (2), 2020 (1) | 5 |
| ID | Kootenai | 2004 (1, 1 EM) | 1 |
| CA | Santa Cruz | 2017 (1), 2018 (1) | 2 |
| CA | Los Angeles | 2003 (1), 2005 (1), 2006(1), 2007 (2), 2009 (1) | 6 |
| CA | Orange | 2005 (1) | 1 |
| CA | San Diego | 2012 (1) | 1 |
| OK | Pittsburg | 2013 (1), 2014 (1) | 2 |
| TX | Travis | 2006 (1) | 1 |
| SC | Charleston | 2014 (1), 2015 (1) | 2 |
| GA | Chatham | 2015 (1) | 1 |
| Total | 63 |
| US State | County | Detection year (number of cases) | Subtotal |
|---|---|---|---|
| WA | Snohomish | 1994 (1), 2018 (1), 2019(1*) | 3 |
| WA | Kitsap | 1994 (1), 2018 (1) | 2 |
| WA | King | 1991(5), 1995(2), 1996(1), 1997(1), 1999(1, 1 EM**), 2015(2), 2016(1 EM) | 13 |
| WA | Pierce | 1991 (4), 1993 (1), 1994 (6), 1995 (2), 1997(1), 2015(4) | 18 |
| WA | Thurston | 1995 (1), 2015 (2) | 3 |
| WA | Clark | 2015 (1) | 1 |
| OR | Columbia | 2006 (1) | 1 |
| OR | Multnomah | 1991 (1), 2000(1), 2005 (2), 2020 (1) | 5 |
| ID | Kootenai | 2004 (1, 1 EM) | 1 |
| CA | Santa Cruz | 2017 (1), 2018 (1) | 2 |
| CA | Los Angeles | 2003 (1), 2005 (1), 2006(1), 2007 (2), 2009 (1) | 6 |
| CA | Orange | 2005 (1) | 1 |
| CA | San Diego | 2012 (1) | 1 |
| OK | Pittsburg | 2013 (1), 2014 (1) | 2 |
| TX | Travis | 2006 (1) | 1 |
| SC | Charleston | 2014 (1), 2015 (1) | 2 |
| GA | Chatham | 2015 (1) | 1 |
| Total | 63 |
Asterisk symbol denotes Lymantria umbrosa.
Detections of AGM in different states of the continental US using disparlure baited traps through CAPS program (EM: Egg mass) *Lymantria umbrosa
| US State | County | Detection year (number of cases) | Subtotal |
|---|---|---|---|
| WA | Snohomish | 1994 (1), 2018 (1), 2019(1*) | 3 |
| WA | Kitsap | 1994 (1), 2018 (1) | 2 |
| WA | King | 1991(5), 1995(2), 1996(1), 1997(1), 1999(1, 1 EM**), 2015(2), 2016(1 EM) | 13 |
| WA | Pierce | 1991 (4), 1993 (1), 1994 (6), 1995 (2), 1997(1), 2015(4) | 18 |
| WA | Thurston | 1995 (1), 2015 (2) | 3 |
| WA | Clark | 2015 (1) | 1 |
| OR | Columbia | 2006 (1) | 1 |
| OR | Multnomah | 1991 (1), 2000(1), 2005 (2), 2020 (1) | 5 |
| ID | Kootenai | 2004 (1, 1 EM) | 1 |
| CA | Santa Cruz | 2017 (1), 2018 (1) | 2 |
| CA | Los Angeles | 2003 (1), 2005 (1), 2006(1), 2007 (2), 2009 (1) | 6 |
| CA | Orange | 2005 (1) | 1 |
| CA | San Diego | 2012 (1) | 1 |
| OK | Pittsburg | 2013 (1), 2014 (1) | 2 |
| TX | Travis | 2006 (1) | 1 |
| SC | Charleston | 2014 (1), 2015 (1) | 2 |
| GA | Chatham | 2015 (1) | 1 |
| Total | 63 |
| US State | County | Detection year (number of cases) | Subtotal |
|---|---|---|---|
| WA | Snohomish | 1994 (1), 2018 (1), 2019(1*) | 3 |
| WA | Kitsap | 1994 (1), 2018 (1) | 2 |
| WA | King | 1991(5), 1995(2), 1996(1), 1997(1), 1999(1, 1 EM**), 2015(2), 2016(1 EM) | 13 |
| WA | Pierce | 1991 (4), 1993 (1), 1994 (6), 1995 (2), 1997(1), 2015(4) | 18 |
| WA | Thurston | 1995 (1), 2015 (2) | 3 |
| WA | Clark | 2015 (1) | 1 |
| OR | Columbia | 2006 (1) | 1 |
| OR | Multnomah | 1991 (1), 2000(1), 2005 (2), 2020 (1) | 5 |
| ID | Kootenai | 2004 (1, 1 EM) | 1 |
| CA | Santa Cruz | 2017 (1), 2018 (1) | 2 |
| CA | Los Angeles | 2003 (1), 2005 (1), 2006(1), 2007 (2), 2009 (1) | 6 |
| CA | Orange | 2005 (1) | 1 |
| CA | San Diego | 2012 (1) | 1 |
| OK | Pittsburg | 2013 (1), 2014 (1) | 2 |
| TX | Travis | 2006 (1) | 1 |
| SC | Charleston | 2014 (1), 2015 (1) | 2 |
| GA | Chatham | 2015 (1) | 1 |
| Total | 63 |
Asterisk symbol denotes Lymantria umbrosa.
Ship at anchorage in Nakhodka, Russia in 2014 with AGM egg masses deposited on the hull and superstructure.
Each of the components of this AGM exclusion effort are an integral contributor to the program’s success. Population monitoring and ship inspections in foreign ports provide US and CA regulatory officials with the necessary information to avoid potential incursions and introductions. Ship inspections and cleaning, if necessary, directly affect the risk of introduction. Fewer ships arriving with AGM life stages lowers the overall risk of introduction. Collaboration from the shipping industries is an important component of this program. The costs for AGM inspections in ports are borne by the shipping industry. Compared to the costs of delaying or losing a ships loading/unloading berth the cost of a ship inspection is relatively small averaging between $3,000 and $8,000. An ocean-going vessel averages between $80,000 to $225,000 a day to operate depending on ship size (Rodrique and Notteboom 2020). Other considerations are contractual obligations for the delivery of products on an agreed date. In addition, ship’s crews trained to inspect their ship during the voyage to North American destinations can further reduce the possibility of AGM introductions. However, egg masses are often located on the exterior surfaces of ships where inspection may not be possible due to access or safety considerations (Fig. 8). Annual monitoring programs in and adjacent to port areas and within inland sites in NA maximizes early detection of an incursion. As with the introduction of any invasive species, early response is crucial to a successful outcome. To date, all detected AGM introductions into North America have been successfully eradicated. The tactics and level of response to a few AGM males captured in traps have been provided by scientists from Federal agencies and State Departments of Agriculture.
The United States supplies trapping materials to several of the overseas agencies and both US and CA representatives meet with their counterparts regularly to address possible program adjustments and to exchange information. The cooperative nature of this program serves as a model for other international regulatory programs. Because international trade has increased dramatically over the past 30 yr the incidence of introductions of pest species and damage has also increased significantly (Simberloff et al. 2005, Roy et al. 2014, Paini et al. 2016, Pyšek et al. 2020). This increased trade has benefited not only the exporting industries but also the consumers with lower costs with wider variability and availability of goods. The question that remains however, is: how can this trade be conducted safely so that introductions of nonnative pest species and their damage is reduced and who is responsible for the costs associated with mitigation and eradication activities when a pest is introduced? In this case importers pay for a portion of the costs through AGM ship inspection fees. Also, another benefit of this program is that it identified other pests that were using the same pathway as AGM. A few of these such as L. mathura, L. monacha, and L. xylina have been rated by APHIS and NAPPO experts as high risk and or species that should be assessed for risk (NAPPO, 2020). However, ships carrying AGM eggs can only threaten a country at ports located in a climatically suitable region (Paini et al. 2018). Paini et al. (2018) recommended countries focus AGM inspection programs towards ships arriving at ports found within climatically suitable regions. Because AGM poses such a high risk of damage to NA and possibly to other regions of the world’s forest resources, the impacts of climate change on its geographic range and contamination of goods and ships from areas previously not considered host countries or countries at risk should be taken into account.
Ecological niche models developed by Peterson et al. (2007) characterized a likely potential invasive distribution of the East Asian strain across the temperate zone of both Northern and Southern Hemispheres excluding deserts and montane regions. Vanhanen et al. (2007) utilizing CLIMEX software predicts a shift in both the southern and northern distribution of both L. dispar and nun moth. Other changes such as CO2 atmospheric concentration may influence interactions between L. dispar, its host trees species, and the trees pathogen (Milanovic et al. 2020). The presence of suitable host(s) is also a factor in determining distribution, however, the synchrony of host bud break with the timing of egg hatch strongly influences survival. Asian strains have a shorter requirement for cold temperatures affecting diapause and a higher percent of hatch without experiencing diapause induced temperatures. This may allow them to invade new temperate areas that would normally be out of synchrony with egg development. Asian strains also survive on significantly more hosts and better utilize marginal hosts in comparison to EGM populations (Baranchikov 1988). Oviposition behavioral characteristics of Asian populations have been shown to influence survival. Extreme temperatures go beyond the limits of the physiological tolerance of wintering eggs (–29. 9°C), and their survival depends on the choice of warm biotopes for oviposition. (Ananko and Kolosov 2021). Ovipositional behavior increases some geographic population’s ability to tolerate temperatures below the egg physiological temperature limits which would be favorably altered in a warmer climate. Other population behavioral differences (larval daily movement, neonate, and adult dispersal etc.) which are not well studied for many of the Asian populations, may impact its ability to establish and populate previously uninfested areas in a warming climate. AGM's flight capability, its expansive host range and phenological attributes all enhance its ability to invade new geographic areas under a warming climate scenario.
Finally, contacts established, and information gathered during this program has enhanced our response to other invasive pests such as the emerald ash borer, Agrilus planipennis (Fairmaire), and the Asian longhorned beetle, Anoplophora glabripennis (Motschulsky). An international approach to invasive species challenges will assist agencies throughout the world in protecting their natural resources.
Acknowledgments
We thank I.M. Asmundsson, J. Levy, T. McGovern, M. Simon, B. Reardon, W.D. Wesela (USDA APHIS), A. Bartuska, R. Flowers, D. Kucera, D. Leonard, J. Space, W. Wallner (USDA Forest Service), W. Asbil, D. Moil, N. Kummen, (Canadian Food Inspection Agency), Y. Kivose, Y. Kim (USDA APHIS International Service), O. Kulinich (All-Russian Center of Plant Quarantine), R. Iwaizumi (Ministry of Agriculture, Forestry & Fisheries, Yokohama Plant Protection Station), H. Lee (S. Korea, Animal Plant Quarantine Agency), Dean Duval (Dept. of Homeland Security Custom & Border Protection). In addition, we thank the Russia – Federal Service for Veterinary and Phytosanitary Surveillance; Republic of Korea - Department of Plant Quarantine, Animal and Plant Quarantine Agency; Japan – Plant Protection Division, Food Safety, and Consumer Affairs Bureau, Ministry of Agriculture, Forestry, and Fisheries; China – Department of Crop Production, Department of Pesticide Management, Ministry of Agriculture and Rural Affairs; USDA APHIS International Service in Tokyo, Japan; Beijing, China; Seoul, S. Korea, and Moscow, Russia and all the vessel inspection companies involved in this program for their support. We thank D. Lance (USDA APHIS PPQ) for his review of an earlier version of this manuscript.
