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Research Article
First record from Italy of the Japanese grape leafhopper Arboridia kakogawana
expand article infoAlessia De Luigi, Francesco Poggi§, Alberto Alma
‡ University of Turin, Grugliasco, Italy
§ Unaffiliated, Missaglia, Italy
Open Access

Abstract

The Eastern Palearctic typhlocybine leafhopper Arboridia kakogawana, feeding on Vitaceae, is recorded for the first time in Italy. In May 2024, adults were detected on yellow sticky traps in three vineyards (Vitis vinifera) in Grugliasco, Chieri and Montalto Dora, province of Turin (Piedmont region). This species, through its trophic activity, causes chlorosis on vine leaves that produce negative effects on the maturation of grapes. However, there are no reports that these insects can transmit phytoplasmas or other pathogens affecting Vitis. The male genital characters useful for its identification are depicted, together with those, for comparison, of Arboridia adanae, the other ampelophagous Arboridia species occurring in Italy.

Key Words

Arboridia kakogawana, grapevine, Italy, pest, Vitis vinifera

Introduction

Arboridia kakogawana (Matsumura 1932) is a leafhopper species (Hemiptera, Cicadellidae, Typhlocybinae, Erythroneurini), native to the Eastern Palearctic region. It was described from Kakogawa City, Honshu Island, Japan (original combination Zygina kakogawana). Later, its presence was detected also in the Korean Peninsula (Dworakowska 1970), the Russian Far East (Anufriev 1971), and, most recently, in China (Cao et al. 2019).

In the Russian Far East (Primorsky Territory), this species inhabits broadleaved and mixed forests and feeds on Vitis amurensis Rupr. (Anufriev 1971), a plant native to Russian Far East, northern and eastern China, Korea, and Japan (Honshu Island) (POWO 2024); thus, the native range of A. kakogawana and that of its primary host plant coincide.

Its first occurrence in the Western Palaearctic, due to accidental introduction, perhaps via cargo ships (Gnezdilov et al. 2008b), was detected in the Krasnodar area of southern Russia in 1999 (Gnezdilov 2000). Later, its presence was reported from North Caucasus (Balakhnina et al. 2009), Rostov region (Artokhin 2009), Crimean Peninsula (Radionovskaya and Didenko 2014), Ukraine (Martynov et al. 2019), Romania (Chireceanu et al. 2019), Bulgaria (Tomov 2020), Serbia (Šćiban et al. 2021), Moldova (Grozdeva 2022), and Hungary (Schlitt et al. 2024), indicating that its range is rapidly expanding westwards.

Arboridia kakogawana feeds as oligophagous on Vitaceae and has so far been found on Vitis sp. and Parthenocissus quinquefolia (L.) Planch. (Chireceanu et al. 2019). It is reported as a pest of cultivated grapevine both in its native area and in invaded regions of Eastern Europe (Chireceanu et al. 2019). The damage is due to intense trophic activity of nymphs and adults in the leaf mesophyll, consequently affecting grape maturation (Gnezdilov et al. 2008a, 2008b).

This study reports the first data on the occurrence of A. kakogawana in Italy (Piedmont region), which currently represents the western limit of its range in expansion.

Materials and methods

The monitoring was conducted on four vineyards; two located in Grugliasco, Turin (we named these two vineyards Agroinnova and Arboricoltura), one in Chieri and one in Montalto Dora (Fig. 1). The area of each vineyard is respectively, 0.37 ha, 0.41 ha, 2.48 ha and 0.05 ha. We installed yellow sticky traps (GLUTOR®, 40×25 cm, Biogard) horizontally on grape branches. We placed three traps in each of the two vineyards of Grugliasco and the one from Montalto Dora and 24 traps in the vineyard of Chieri, depending on the hectares of each one. Traps were replaced every two weeks. The period of observation went from the end of April to mid-October 2024. We also monitored the vineyards every week to observe the presence of nymphal stages and adults. The specimens we collected by traps were deposited in the Department of Entomology of Grugliasco and then examined through the observation of the aedeagus to identify the species. Some nymphs and adults captured in field were also photographed to observe and describe in detail the morphology.

Figure 1. 

Areas of the four vineyards investigated: A. Chieri; B. Arboricoltura; C. Agroinnova; D. Montalto Dora.

For the study of genital characters, the entire male abdomens of the examined specimens were dissected out and macerated in 10% KOH solution at approximately 55 °C for about 20 minutes until clarification. The cleared material was subsequently washed in distilled water and transferred to glycerol for observation and further dissection. Finally, the genital pieces were mounted on a slide in dimethyl hydantoin formaldehyde (DMHF) medium.

The drawings of the male genitalia were made by means of a Laboval-4 microscope with drawing tube attachment. The photos of the specimens were taken with SnS-System (MJKZZ, Europe) fitted with a Canon 90D (Canon Inc., Tokyo, Ota, Japan). This system was connected to a computer where the Focus Stacking Studio software (FSS, MJKZZ, Europe) was installed to control the SnS-System.

The image processing and plate composition of the drawings were made by means of MAGIX Xara Photo & Graphic Designer 19.0.1.65946 software. The illustrations are all original.

The morphological terminology follows Dietrich (2005) and Dietrich and Dmitriev (2006).

Results

Records

Through the study of male genitalia, we identified several individuals as Arboridia kakogawana. We found specimens in each vineyard we monitored. In detail, we obtained from the traps: 216 individuals from Arboricoltura, 868 from Agroinnova, 268 from Chieri, and 112 from Montalto Dora (Table 1). We also calculated the average number of catches per trap. For Arboricoltura the average was 5.53 adults per trap, for Agroinnova was 22.25, for Chieri 0.93 and for Montalto Dora 4.66.

Morphological notes

The habitus of Arboridia kakogawana (Fig. 2A) is similar to the other Arboridia species occurring in Europe, and can only be reliably distinguished by male genital morphology. Adult body length: 2.6–3.1 mm. The intensity of the coloration of individuals, particularly in forewings and pronotum, is very variable, from pale to darker. The nymphs (Fig. 2B) are entirely light yellowish green, with blunt dark setae on dorsal side of head, pronotum, mesonotum, metanotum, forewing pads, and abdomen. The most important genital characters to distinguish the species are the shape of aedeagus (Fig. 2C, D), styles (Fig. 2F), and pygofer processes (Fig. 2E), with characteristic bifurcated apex. In particular, the aedeagus has a single spiniform ventral process on the preatrium, close to the base of shaft (Fig. 2C, D), highly variable in length in different individuals, whereas most of the Arboridia species have a pair of processes, of various shapes according to different taxa.

For the purpose of an immediate comparison, we provide the figures (Fig. 3A–D) of the male genital characters of the other ampelophagous Arboridia species occurring in Italy, namely, Arboridia adanae (Dlabola 1957), which is distributed in the Balkans, Anatolia, and the Middle East, and first detected in Italy, in the Apulia region, in 2021 (Piccinno et al. 2024).

Table 1.

Number of adults of Arboridia kakogawana collected by yellow sticky traps in 2024.

Total no. of Arboridia kakogawana adults
Date Chieri Agroinnova Arboricoltura Montalto Dora
30-04-24 0 0 0 0
17-05-24 0 0 0 0
30-05-24 4 4 0 0
13-06-24 0 0 0 0
26-06-24 0 0 0 0
15-07-24 48 0 0 0
25-07-24 44 60 0 12
06-08-24 4 56 0 0
20-08-24 0 44 20 12
04-09-24 36 360 144 16
20-09-24 48 160 24 64
03-10-24 16 72 16 8
15-10-24 68 112 12 0
TOTAL 268 868 216 112
Figure 2. 

Arboridia kakogawana (specimens from Italy, Piedmont): A. Adult; B. Fifth instar nymph; C. Aedeagus, lateral view; D. Aedeagus, ventral view; E. Left pygofer process, lateral view; F. Left genital style, ventrolateral view.

Figure 3. 

Arboridia adanae (specimens from Italy, Apulia): A. Aedeagus, lateral view; B. Aedeagus, ventral view; C. Left pygofer process, lateral view; D. Left genital style, ventrolateral view.

Host plants and life cycle

The first adults of Arboridia kakogawana were observed in field at the end of May. We found specimens on the following varieties of Vitis vinifera: Freisa, Bonarda, Malvasia, Chardonnay, Montanera, Nebbiolo, Pinot, Moscato.

The presence of nymphal stages of A. kakogawana was observed from the second half of July to the first half of October.

As reported in article 097 of the EPPO Reporting Service (2016), during the monitoring season we observed two peaks of the population as in Krasnodar. One peak was reported in the second half of July and one in early September (Fig. 4). The presence of adults was observed till the first half of October.

Figure 4. 

Population trend of Arboridia kakogawana adults in 2024.

Phytosanitary issues

From literature we know that nymphs and adults of Arboridia kakogawana feed mainly on the lower side of the leaves, causing the loss of photosynthetic green pigments. As a result of sucking the affected tissue becomes chlorotic and on the upper side of the leaves appear the discolored zones. The spots are disposed along the central vein and, in case of severe attacks, are placed over the entire surface until merging and forming large chlorotic zones (Chireceanu et al. 2019). As a result, premature yellowing of leaves produces a negative effect on the maturation of grapes (Gnezdilov et al. 2008a).

In the monitored vineyards, we did not find such damage, apart from a few depigmentation spots on the leaves. Since several typhlocybine species have been found in the same vineyards, such as Erasmoneura vulnerata (Fitch 1851), we cannot state with certainty that these spots are exclusively due to A. kakogawana.

Final remarks

Arboridia kakogawana is the third exotic typhlocybine species feeding on Vitis introduced in Italy in recent years, after the Nearctic Erasmoneura vulnerata, detected first in 2004 by Duso et al. (2005), and the East-Mediterranean Arboridia adanae (Dlabola 1957), detected first in 2021. These three species have been added to the ampelophagous typhlocybine leafhoppers already occurring in Italy, namely, Hebata vitis (Göthe 1875), Jacobiasca lybica (Bergevin & Zanon, 1922), and Zygina rhamni Ferrari 1882. Although A. kakogawana does not seem to have caused any particular damage in the vineyards, monitoring its range of expansion is recommended.

Acknowledgements

We thank Valerio Mazzoni (Fondazione Edmund Mach, S. Michele all'Adige, Italy) for providing us with specimens of Arboridia adanae, Francesco Tortorici (DISAFA, Dipartimento di Scienze Agrarie, Forestali e Alimentari, Grugliasco, Italy) for helping us with the photographic material of Arboridia kakogawana specimens and the research technician Enrico Busato (DISAFA, Dipartimento di Scienze Agrarie, Forestali e Alimentari, Grugliasco, Italy) for helping us with the identification, examination and photographic material of A. kakogawana specimens.

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