Lycorma delicatula
(spotted lanternfly)

Lycorma delicatula, also known by the common name spotted lanternfly (SLF), is an economically damaging plant pest native to China and Southeast Asia. SLF has been introduced in recent history to the Republic of Korea, Japan and most recently, the USA. It has become a major agricultural pest and nuisance pest in both Korea and in the USA. Feeding has been recorded from over 100 hosts and damage from this pest impacts numerous types of fruit trees, vines, specialty crops, ornamental plants and native vegetation in its introduced ranges. Feeding damage can reach serious levels in agricultural settings reducing yield, plant vigour, fruit quality and eventually host mortality. L. delicatula causes indirect damage to plants by excreting large quantities of honeydew on and around host plants which causes additional problems for crops, gardens and ecosystems. In the USA, SLF is currently only present in the Mid-Atlantic region but is continuing to spread both naturally and by human assisted means.

If L. delicatula reaches a new environment, the risk of introduction in novel habitats increases as the insect develops. After emerging, nymphs will spread out in the environment seeking food sources. This movement is localized and nymphs are not particularly hardy, limiting their spread and risk of accidental transport. When it reaches adulthood, spotted lanternfly (SLF) can exhibit migratory flights of short distances that are repeated multiple times (Domingue and Baker, 2019). These flights can land SLF in vehicles and anthropogenically distribute the pest moderate distances, especially in cargo vehicles with exposed goods or train cars. Gravid SLF transported by these methods can quickly establish new population as females can lay up to 3 or more egg masses for potentially 150 or more SLF in the following year. However, the adults are very conspicuous and can easily be recognized by the public when educated (Urban, 2020).

The greatest risk of L. deliculata spreading to new countries comes from the egg stage. The eggs are laid in masses of approximately 30-50 eggs and covered with a waxy protective coating (Dara et al., 2015). This coating is dull in colour, starting white when fresh and ranging from light to dark grey when dried. Over time, it can take on the appearance of dried mud helping to camouflage it. Egg masses are laid on a number of inanimate objects including vehicles, metals, artificial and natural surfaces and quarry products as well as on timber and nursery products. Goods that are stored outdoors in SLF areas during the egg laying season pose a substantial risk as egg masses can be deposited while awaiting transportation. These egg masses can remain dormant for long periods allowing survival through long ocean voyages. Nymphs and adults do not overwinter or have the reserves to survive ocean vessel travel and air transport is likely unhospitable as well limiting the long-distance delivery of mobile life stages.

The global risk of L. delicatula introductions includes possible regions on six continents (Jung et al., 2017; Wakie et al., 2020). One of the preferred hosts, Ailanthus altissima (tree of heaven), is a common and widely distributed invasive tree in much of the world providing a familiar and important host upon invasion. Additionally, the broad host range of herbaceous plants, vines, woody shrubs and trees, either cultivated or wild, increase the risk of establishing SLF upon arrival. Grape (Vitis vinifera) vineyards also appear to be particularly attractive to SLF and regions that grow grapes overlap well with SLF’s predicted global distribution overlapping the western USA, parts of South America, Australia, southern Africa and much of Europe.

In the USA, the insect is under a series of quarantine orders from both infested and uninfested states. Canada and Morocco have listed it as a quarantine pest and it is included it in the EPPO A1 List by the European and Mediterranean Plant Protection Organization.

Lycorma delicatula utilizes a wide variety of hosts and therefore use no special habitat, however they are often observed on roadsides and waste areas, particularly where tree-of-heaven (Ailanthus altissima) and/or wild grapes (Vitis) occur as well as in vineyards.

It is important to note that many of the plant species recorded as hosts by publications are exclusively known as egg deposition substrates. L. delicatula also lay their egg masses on non-natural structures and materials, so their presence on living material should not necessarily be interpreted as suitable habitat. They may, however, serve as a guide for survey, detection and inspection duties for this pest.

Many of the crops listed here have experienced varying levels of damage from Lycorma delicatula. Orchard crops can see large influxes of adults into them onto crops, creating small but possibly damaging windows through feeding pressure and indirect damage to crops through honeydew. Damage to orchard trees has not yet been quantified and exact damages are mostly estimates or potential (Parra et al., 2018; Harper et al., 2019).

Lycorma delicatula is a univoltine species in its native and introduced ranges. Egg masses overwinter and gradually emerge in the spring (April to May in the USA). Often the egg masses are laid on or near host species but can also be found laid on inanimate substrates or non-host plants. The nymphs emerge from their egg masses and disperse into the environment in search of appropriate hosts. The nymphs display cyclic behaviour of falling or leaving hosts and returning to or moving onto new hosts (Kim JaeGeun et al., 2011). The known host range of L. delicatula is the broadest at this time. Many herbaceous host plants fed upon by early instars are probably not large enough to support later instars and adults. Nymphs in the first to third instar are black with white spots and remain similar in appearance while growing larger with each instar.

The fourth instar of L. delicatula undergoes a dramatic change in appearance, with red featuring predominantly, replacing the black with white spot colouring of the first three instars. This colouration is thought to be aposematic in nature as the spotted lanternfly starts narrowing its host range, which includes Ailanthus altissima. This tree (along with other hosts) contains compounds that decrease the palatability of the insect to predators (primarily birds) (Kang et al., 2017).

The adult’s life stage appears in late summer and limited feeding patterns and sex-determinate behaviours emerge (Baker et al., 2019). Adults will focus on woody tree material for food sources as smaller plants cannot sufficiently support them. Large vines, such as grapes (Vitis vinifera) in vineyards, also become attractive to adults (Leach and Leach, 2020). Males and females will segregate in the wild, aggregating on separate trees as they feed. Later in the autumn both sexes will intermingle and mating will occur, with female mating with multiple males.

Females will start laying eggs around September in the USA on a wide variety of substrates (Dara et al., 2015). Smooth-barked trees are most common, but flat artificial structures, metal surfaces, vehicles, outdoor furniture and equipment, rocks, nursery materials and other substrates can all host egg masses. Egg masses can be found in a clustered arrangement with multiple females laying in the same area or adjacent to egg masses of other females (Liu, 2020). Egg laying persists until the late autumn when cold weather kills the adults, generally after the weather consistently reaches freezing overnight temperatures.

Genetics

The genetics of L. delicatula invasions have been explored in both Asia and the USA. In Asia, the introduction of spotted lanternfly to Korea and Japan were matched to populations of L. delicatula in China, linking their introduction from areas around Beijing, Tianjin, Quingdao and Shanghai (Kim et al., 2013). The genome of a wild-collected individual from Berks County, Pennsylvania, USA was recently assembled and published along with improvements to sequencing protocols (Kingan et al., 2019) that make efforts to assess the population genetics of the USA population much more attainable. Such an assessment has not yet been made.

Reproductive Biology

Adult L. delicatula segregate to some degree after emerging by sex (Baker et al., 2019). As the mating period approaches, the two sexes will start to form gregarious congregations. Large migratory flights can be seen by both sexes with mating following this dispersal period (Baker et al., 2019). Mating can occur multiple times after a brief courtship and copulation can last up to 4 h. Female abdomens will start to swell after mating as egg development matures. This swelling will present as yellow tissue between swollen abdominal sections. Egg laying by females can results in multiple egg masses.

Eggs undergo diapause early in their embryonic development, requiring 2 weeks of warm temperatures before hatching was induced (Shim and Lee, 2015). Eggs that overwinter for longer periods (5 months) have better synchronous hatching, as well as more successful hatch rates, suggesting that colder temperatures are beneficial to the survival of the eggs (Shim and Lee, 2015).

Nutrition

L. delicatula has been found to feed on over 100 plant taxa across 33 families (Barringer and Ciafre, 2020). The nymphs have a broader range of hosts than their adult’s counterparts. Later instars and adults have a narrowed feeding range and move onto physically larger hosts to support their nutritional needs and to possibly uptake defensive chemicals (Kang et al., 2017). L. delicatula shows a strong preference for Ailanthus altissima, though they can complete development in the absence of this species and often utilize multiple hosts through their development (Uyi et al., 2020).

Environmental Requirements

Environmental requirements based upon work using Climex predictions have been used to determine preferred and tolerated status (Jung et al., 2017).

A few natural enemies of Lycorma delicatula have been identified. Egg parasitoids include Anastatus sp. (Hymenoptera: Eupelmidae) in Korea Republic and Ooencyrtus kuvanae (Hymenoptera: Encyrtidae) in the USA (Liu and Mottern, 2017). It is unclear if the Anastatus spp. is a specialist while Ooencyrtus is known to parasitize many species. Dryinus browni is also being studied as a biocontrol agent as it is present in the home range of spotted lantern fly in China and parasitizes L. delicatula (Hoelmer et al., 2019). Generalist predators have also been found in the USA but probably have little impact on the populations (Barringer and Smyers, 2016).

Medicinal, pharmaceutical

• Traditional/folklore

Lycorma delicatula can be detected visually throughout the growing season. The nymphs in the first three instars are often overlooked by the general public, either because of their small size, bland colouration, or similarity to other small dark insects. The fourth instar and adult are very conspicuous in contrast (Urban, 2020). The general public, with education, can reliably identify and report this pest in the environment and around their homes. Identification of egg masses by the public is less reliable due to their cryptic colouration like dried mud and the habit of them being laid in protected, covered spaces or high on structures and trees.

Visual surveys in the spring focus on more herbaceous plants and younger branches of host trees as nymphs require the softer tissues to feed. Branch tips, small shoots and fresh regrowth are most likely to yield detections. As L. delicatula reaches the fourth instar, they migrate to a smaller range of woody hosts, particularly Acer, Ailanthus, Juglans and Vitis in the USA (Urban, 2020). Orchard survey for spotted lanternfly should be focused on hedgerows and periphery for most of the year until the late autumn when it is more likely to migrate to feed.

Visual survey for eggs can be done anytime between September and May in the USA. Egg masses will persist through this entire period and occasionally older egg masses from the previous season can be found, indicating that the infestation is at least 1 year old. Egg mass inspections should focus on materials that are stored outdoors during egg laying season, roughly September to November or December, based on weather conditions killing adults. Egg masses can be laid on a variety of surfaces including bark, stone, wood, metal, plastic and stiff fabrics. Egg masses are also laid on open, exposed surfaces as well as tight spaces such as undersides of vehicles, furniture, stone goods and under tree bark making detection difficult.

In North America, there are no other fulgoroids that closely match Lycorma delicatula. In the northeast, only one true Fulgoridae occurs, which is completely black (Bartlett et al., 2014). Other fulgorid species occurring in the south and southwest USA are much smaller and dully coloured in comparison. Adult L. delicatula may superficially resemble some moths, particularly noctuid underwings, due to their colourful hindwings.

Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

Public Awareness

Public awareness campaigns in the USA have been very successful due the striking features, large size and gregarious behaviour of spotted lanternfly. The public can reliably identify fourth instars and adults.

Eradication

Eradication and suppression are being attempted in the USA using a combination of quarantine and chemical and mechanical controls (Dara et al., 2015; Urban, 2020). The original methodology by the Pennsylvania Department of Agriculture utilized trap trees of Ailanthus altissima treated with a systemic pesticide, leveraging the preference of spotted lanternfly for this plant in the autumn. This was coupled with removal of other, non-treated A. altissima trees in the area concentrating L. delicatula to these trap trees. However, efforts failed to completely contain the pest and it has continued to spread across the Mid-Atlantic. Treatment efforts have continued to be modified transitioning to target more species of trees, different chemical products and different application methods.

Other eradication methods that are coupled with chemical controls included egg mass scraping to manually destroy eggs, sanitation of waste products that might harbour egg mass by chipping landscape waste or incinerating green wastes, and banding trees and posts with adhesive tape.

Chemical Control

A variety of chemicals have been shown to have some control (Leach et al., 2019). Chlorpyrifos was most effective for egg masses with rates of 100% mortality. Nymphs and adults were susceptible to multiple classes of insecticides including carbamates, organophosphates, neonicotinoids and pyrethroids, with differing classes having variable residual control. Additional control with fungal pathogens is also being examined using Beauveria bassiana and Batkoa major (Urban, 2020).

Monitoring and Surveillance (Incl. Remote Sensing)

Passive survey tools involve tree bands, which are glue-coated sheets of paper wrapped around the trunks of host trees or vineyard posts. These capture spotted lanternfly migrating across the host tree trapping it on the sticky surface. Proper installation should be taken to ensure that bycatch, especially of vertebrates, is limited to minimize impacts to the environment and for positive public relations. Pheromone trapping and other methods of baited traps have had limited success currently using methyl salicylate, (Z)-3-hexenol and (E,E)-alpha-farnesene (Cooperband et al., 2019). Physical traps using lures that have been effective are modified pecan weevil trap, or circle trunk trap, which have been effective in areas at high density (Nixon et al., 2020).

There is a need for detection tools that can be deployed at low density infestations that can reliably capture L. delicatula or signs of. Currently, tools are limited and the lack of specific pheromones (which are unknown in Fulgoroidea) or chemical attractants, means trapping lacks a level of specificity (Derstine et al., 2020; Urban, 2020). Environmental DNA is being developed for spotted lantern fly, though it has not been widely deployed (Valentin et al., 2020).

Basic biological information is required on the behaviour, host use patterns and range, movement in the environment, dispersal mechanisms, reproductive and fecundity limits and population dynamics of L. delicatula. Prior to its introduction to Korea, there was limited information on the biology of L. delicatula in the native range. The host range is likely to expand in number as L. delicatula moves south and westwards in the USA and encounters more temperate and tropical potential hosts. Additionally, host risk assessment for other suitable habitats such as the western USA, Europe, Africa and Australia would also be beneficial if the pest arrives (Jung et al., 2017).

Additionally, understanding the host requirements for development of L. delicatula will be important in both survey, detection and control. Ambiguity still exists on what hosts, if any, are critical for their complete development and better understanding of this will influence future predictions of the possible spread and introduction of spotted lantern fly (Uyi et al., 2020).

Understanding the behaviours of L. delicatula in the environment, at both low and high population density, will be valuable in determining the risk of spread accidentally (Baker et al., 2019). The heterogenous presence of spotted lantern fly in the environment also provides challenges in making management decisions and ensuring negative detections. Adults, when at higher density start making dispersal flights which can place them in situations where they may be transported long distances, i.e. train cars, truck beds, planes, or other conveyances (Baker et al., 2019. By understanding when these conditions arise, cultural changes to business and lifestyle practices can be implemented to limit the chance of long-distance dispersal.

Treatment methods for control and eradication with limited non-target effects will be of interest if chemical controls continue to be a tool used in current infestations or if the pest is discovered elsewhere (Leach et al., 2020). Current treatments focus on introduced hosts, Ailanthus altissima, which have limited uses for native, non-target species. However, now that L. delicatula is known not to be required for development, this strategy should be re-evaluated for efficacy (Uyi et al., 2020).

Biocontrol for long term management will be crucial as current methods of control are costly, time and labour intensive, and limited in scope. Passive methods of specific biocontrol will need to be developed to control outbreak populations as it spreads across the USA. While natural predators and introduced parasitoids have been found to attack L. delicatula, they probably will have minimal effect as generalists (Barringer and Smyers, 2016; Liu, 2019).

USA: United States Department of Agriculture Animal and Plant Health Inspection Service, USDA APHIS, 4700 River Road Riverdale, MD 20737 USA, https://www.aphis.usda.gov/aphis/home/

10/11/20 Original text by:

Lawrence Barringer, Pennsylvania Department of Agriculture, 2301 N. Cameron St., Harrisburg, PA 17110 USA