Review article
A review of biology and management of Lycorma delicatula (Hemiptera: Fulgoridae), an emerging global invasive species

https://doi.org/10.1016/j.aspen.2019.03.004Get rights and content

Highlights

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    Lycorma delicatula (White) (Hemiptera: Fulgoridae) is an emerging invasive species.

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    Lycorma delicatula is known to attack at least 65 host plants.

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    For monitoring this pest, visual survey has been the primary means

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    Chlorpyrifos, dinotefuran, and etofenprox are effective against this pest.

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    Natural enemies in the genus Anastatus and Dryinus are promising candidates.

Abstract

Lycorma delicatula (White) (Hemiptera: Fulgoridae) is an invasive species inflicting damage to agricultural and forest systems. This species is native to China, Taiwan, and Vietnam. Lycorma delicatula was accidentally introduced into South Korea and Japan, with outbreaks reported since mid-2000s. More recently, this pest was found in Pennsylvania, USA, and its geographical distribution has steadily expanded since the introduction with increasing population densities in the USA. This species is univoltine in invaded regions and overwinters in the egg stage. Lycorma delicatula is known to attack at least 65 host plants, and so-called preferred host plants such as Ailanthus altissima and Vitis vinifera are present in all invaded countries. This species threatens grape industries in China, South Korea, and USA, with the impact on other crops still unknown, at least in the USA. For monitoring this pest, light or pheromone traps have not yet been developed, but using sticky tree bands may serve as a promising tool. To date, visual survey is the primary means for detecting L. delicatula and studying their population dynamics. To control L. delicatula, several studies evaluated conventional insecticides. Under field conditions, chlorpyrifos, dinotefuran, etofenprox, and etofenprox + diazinon yielded high levels of mortality against this pest. In general, environmentally-friendly materials, registered as Environmentally-Friendly Agricultural Material in South Korea, resulted in lower insecticidal efficacy against L. delicatula compared with conventional chemicals. Natural enemies of L. delicatula such as egg parasitoids in the genus Anastatus and Dryinus are promising candidates as a long-term solution for management.

Section snippets

Invasion dynamics

Lycorma delicatula (White) (Hemiptera: Fulgoridae) is a plant hopper native to China, India, and Vietnam (Jung et al., 2017). Although L. delicatula was initially reported from Shanxi, Shandong, and Hebei provinces in China (Liu, 1939), recent surveys have confirmed that this species is distributed throughout China and other countries including Taiwan, Vietnam, and India (Xiao, 1992; Hua, 2000).

In 1930s, a Japanese researcher mistakenly reported that L. delicatula occurred in Korea (Doi, 1932a

Egg

In South Korea and Pennsylvania, USA in which L. delicatula is univoltine (Lee et al., 2014; Dara et al., 2015), eggs are laid from September until early November (Park et al., 2009; Lee et al., 2011a; Lee et al., 2014; Dara et al., 2015). However, it is possible that this species becomes multivoltine in warmer climate zones such as the southern part of the USA. The size of egg was on average 2.57 and 1.36ā€Æmm in length and width, respectively (Park et al., 2009). In invaded areas, eggs

Dispersal

Nymphs often engage in a cyclical ascending-falling behavior on host plants; on Betula platyphylla (Betulaceae), nymphs repeatedly ascended trees after having fallen to the ground in response to physical stimuli such as wind (Kim et al., 2011b). As nymphs develop, each ascending-falling cycle becomes longer in duration as the arolium (i.e., adhesive pad on the pretarsus) becomes larger; the size of this structure is an important determinant for L. delicatula climbing ability (Kim et al., 2011b

Overwintering

Successful overwintering of L. delicatula is crucial for populations to establish and expand their geographical ranges in newly invaded regions. This species overwinters in the egg stage; egg masses can be found as early as in September in South Korea (Park et al., 2009; Lee et al., 2011a; Lee et al., 2014) and Virginia and Pennsylvania, USA. Overwintered eggs remain unhatched in the field until Aprilā€“May or later the following year in invaded areas (Park et al., 2009; Lee et al., 2011a; Choi

Behavior

Feeding behaviors of L. delicatula was investigated using electrical penetration graph (EPG) on seven plant species: Ailanthus altissima (Simaroubaceae), Vitis vinifera (Vitaceae), Pinus densiflora (Pinaceae), Hibiscus syriacus (Malvaceae), Malus pumila (Rosaceae), Pyrus calleryana (Rosaceae), and Prunus persica (Rosaceae) (Lee et al., 2009). This technique has been widely used to study feeding behaviors of plant-sap feeding hemipterans (McLean and Kinsey, 1967; Backus et al., 2017). In the

Host plants

Several studies in the native and invaded areas have reported a variety of host plants of L. delicatula based on field surveys and literature review (Han et al., 2008; Park et al., 2009; Barringer et al., 2015; Dara et al., 2015). In China, at least 23 plant species including Ailanthus altissima (Simaroubaceae), Actinidia chinensis (Actinidiaceae), Malus sp. (Rosaceae), Prunus mume (Rosaceae), P. persica, P. salicina, Robinia pseudoacacia (Fabaceae), and Vitis vinifera (Vitaceae) have been

Damage & economic importance

Lycorma delicatula damage plants directly by feeding plant sap as well as indirectly by excreting large amount of honeydew which can cause sooty mold and interfere photosynthesis (Dara et al., 2015). In China, L. delicatula is reported as a pest of diverse shrubs and trees including tree of heaven (Ailanthus altissima), Chinese Mahogany (Toona sinensis), white cedar, black locust (Robinia pseudoacacia), cottonwoods, willows (Salix spp.), grapes (Vitis spp.), and apples (Malus spp.) (Xiao, 1992;

Monitoring tools

To date, no standard monitoring trap exists for L. delicatula and visual inspection has been employed as a main survey method to monitor and study population dynamics of this insect (Han et al., 2008; Park et al., 2009; Lee et al., 2011a; Lee et al., 2014; Barringer et al., 2015). However, several studies have reported attractive stimuli and dispersal behaviors which can serve as foundational information to develop effective monitoring tools for L. delicatula.

First, like many other insects, L.

Chemical control

Several studies evaluated the effectiveness of insecticides against L. delicatula in South Korea (Park et al., 2009; Kim et al., 2010; Shin et al., 2010; Lee et al., 2011a; Choi et al., 2012a) (Table 1). For nymphs, a laboratory bioassay demonstrated that both 1st and 2nd instars were highly susceptible to 26 insecticides when sprayed directly on the insects at recommended rates (Shin et al., 2010): all of the tested insecticides including five organophosphate, two carbamates, four pyrethroids,

Biological control

Natural enemies of L. delicatula are promising candidates for a long-term management strategy against this invasive species (Kim et al., 2011c; Choi et al., 2014; Yang et al., 2015; Barringer and Smyers, 2016; Liu and Mottern, 2017). Recent field surveys have found that egg parasitoids of L. delicatula are present in China (Yang et al., 2015), South Korea (Kim et al., 2011c; Choi et al., 2014), and the USA (Liu and Mottern, 2017). Among egg parasitoids, the genus Anastatus (Hymenoptera:

Behavioral control

Response of L. delicatula to potential attractants or repellents could be incorporated into management programs against this pest. Repellent effects of 10 essential oils (5ā€ÆĪ¼L doses) to 4th instars of L. delicatula were evaluated using an olfactometer and only lavender oil resulted in significant repellency (Yoon et al., 2011). This essential oil could be used in developing a push-pull strategy to behaviorally manage L. delicatula populations. In addition, a recent study demonstrated the

Conclusions

Lycorma delicatula is a planthopper native to China, India, Taiwan, and Vietnam and this species has recently emerged as a serious invasive species especially in South Korea and the USA. Climatic conditions and host plants present in these invaded regions provide suitable environments for L. delicatula to establish and spread. Indeed, this invasive species has rapidly expanded its geographical distribution with reports of much greater densities being present. As predicted based on the host

Acknowledgements

We thank Fumin Wang (West Virginia University) for his help translating Chinese literature for the manuscript. This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2018R1D1A1B07046061).

Conflict of interest

No conflict of interest exists in the submission of this manuscript and manuscript is approved by all authors for publication.

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