First occurrence of Halyomorpha halys in Bordeaux vineyards

Here we report the first detection of Halyomorpha halys (Stål, 1855) in Bordeaux vineyards. The species is native to Eastern Asia and was introduced to France in 2012. Halyomorpha halys is highly polyphagous and causes significant damage to various crops, including grapevines. From 2018 to 2020, Pentatomidae species were collected in vineyards in the Bordeaux region. In 2020, the first nymphs and adults of H. halys were identified in the plot centres. The study emphasizes the need for field population monitoring in risk assessment and, consequently, risk management.

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INTRODUCTION
The number of invasive species continuously increases worldwide (Simberloff et al., 2013) and this is primarily attributed to human trade and transport.As their numbers increase, these species can have ecological and/or economic implications; but eradicative or corrective measures can be implemented in response (Renault et al., 2021;Simberloff, 2003;Simberloff et al., 2013).In Europe, the trade of fruits presents an entry channel for exotic pests (Suffert et al., 2018) and thus poses a particular risk.
During phytosanitary import inspections over the past twenty years, many invasive insects have been detected or intercepted from different regions of the world in France (Balmès and Mouttet, 2019;Mouttet et al., 2020;Touroult et al., 2016).Among these, some were not detected or intercepted, as was the case for the dramatic introduction of the Asian yellow-legged hornet (Monceau et al., 2014) or of Drosophila suzukii Matsumara.
H. halys was detected for the first time in Europe in 2004 in Liechtenstein and the first outbreaks were declared in 2007 in Zurich, Switzerland (Wermelinger et al., 2008).In France, the first record dates back to 2012 in the Alsace region (Callot and Brua, 2013;Streito et al., 2014).Since then, this insect has spread through the country and its presence was reported in 2013 in Paris (Garrouste et al., 2014), in 2015 in Toulouse and the Landes region (located in the south of Bordeaux) (Labatut and Géry, 2019) and in 2018 in urban areas near Bordeaux (Maurel et al., 2016;Streito et al., 2020).
Grapevines are some of the most important crops cultivated in the Bordeaux region and are also one of the host plants of H. halys.Indeed, in North American vineyards, all development stages can be found on the plants, from eggs to adults (Basnet et al., 2015).Nymphs and adults feed on and damage the grapes (Smith et al., 2014).Damage can be observed in the vineyard and/or in derived products (Nielsen et al., 2016).By feeding on the fruit with its mouthparts, injecting saliva and sucking up the plant fluid, the insect causes declines in the quality and yields of grapes, especially post-veraison (Basnet et al., 2015;Smith et al., 2014).Moreover, damages to the berries may lead to aromatic deviations in the wine.If bugs are collected along with clusters and transported in bins to wineries, which is possible for nymphs, they can impact the odour or flavour of the product when crushed along with the berries.The presence of released defensive odours can change the flavour of the wine and is detectable by humans (Kehrli et al., 2021;Mohekar et al., 2017;Pfeiffer et al., 2012).
For the Bordeaux region, at this time, no Pentatomidae was referenced as a clear pest to grapevines (Boudon-Padieu et al., 2000).However, populations of H. halys are constantly increasing in the south of France (Hamidi et al., 2019;Streito et al., 2020) and are becoming a major concern for French winegrowers.Monitoring is required to deploy anticipatory control strategies against the pest.The study aimed to collect individuals from the stink bug community in vineyards and surrounding hedges in the Bordeaux region to detect the presence of H. halys.

Study sites
The experiment was conducted in conventional Merlot grapevines for wine production.Plots were located in the Bordeaux region, within a 5 km radius from the city of Libourne, France and were designated as follows: Pomerol

Monitoring and identification of Pentatomidae species
From 2018 to 2020, adults and nymphs were collected in spring (mid-May), summer (mid-July) and before the harvest (end of August).At each sampling date, insects were collected by beating techniques in the morning at cooler temperatures when insects were relatively motionless (Muneret et al., 2019).In grapevine plots, two transects of ten vines each were sampled.On each transect, sampling was carried out on one side by sampling five vines on one row, then completed by sampling the same number of vines on the opposite row.Only one transect was carried out over an equivalent length of 20 vines on one side only and this was performed in the border exposed on the vineyard side.
Stink bugs were collected and stored in 70 % alcohol and identified under a stereomicroscope in the laboratory.Insects were counted and their phenological stages were determined according to the identification key of French Pentatomidae (Lupoli and Dusoulier, 2015).

RESULTS
In the vineyard centre, 18 Pentatomidae specimens were collected (Table 1).Almost all H. halys specimens collected in the fields were nymphs.Halyomorpha halys specimens were collected in 2020, while none were observed in 2018 and 2019 (Table 1).Field observations showed that eggs of H. halys were present under grapevine leaves (personal observations, Rouzes) (Figure 1).Therefore, all stages were found in the vineyards analysed.Additionally, adults and nymphs were observed on grapevines close to vineyards close to harvest in 2020.

DISCUSSION
The present study highlights the establishment of the exotic pest species H. halys in the Bordeaux vineyard area.However, according to observations, the population is currently relatively low.The pest was recently introduced in France and its population is quickly increasing across the country (Streito et al., 2021), raising concerns to farmers.
Our observations indicate that H. halys arrived in the Bordeaux vineyards in 2020.The presence of nymphs in the centres of all three sampled plots shows that the insect is well-established.It is well-known that H. halys needs to feed on different host species to complete its life cycles (Acebes-Doria et al., 2016), leading to the movement of adults and nymphs throughout the landscape (Acebes-Doria et al., 2017;Blaauw et al., 2019;Nielsen and Hamilton, 2009).Hedges and crops surrounding the vineyards include several alternative host plant species, such as tree of heaven, kiwis, apples, maples, plums and hazel trees, particularly conducive to the establishment of this pest (Haye et al., 2014;Hedstrom et al., 2014;McPherson, 2018).A rise in edge populations is expected and should therefore be monitored.The phenomenon is known as the border effect (Basnet et al., 2015) or spillover (Tscharntke et al., 2005).Nonetheless, the low number of individuals and the limited diversity recorded of bugs in the plots allow the vineyard plot to be deemed an ecological zone not well adapted to most of these species.These pentatomids are otherwise only observed as adults.
Palomena prasina was cited as a very occasional pest in southeastern France and around the Mediterranean (Galet, 1982); the species is currently an emerging pest in southern France but mainly affects apples and hazelnuts (Hamidi et al., 2022;Streito and Bout, 2019).Nezara viridula is an exotic pest species currently on the rise in France (Streito and Bout, 2019) but not referenced as a serious pest of grapevines (McPherson, 2018).Eurydema oleracea was also captured, but only in the edge samples, and the species is known to feed on mainly cruciferous plants species (Piersanti et al., 2020).Rhaphigaster nebulosa, D. baccarum, C. purpureipennis and N. viridula are common hedge species of surrounding vineyards and not mentioned as pests of grapevines (Franin et al., 2021).Until the present study, and according to previous knowledge, no Pentatomidae species was referenced as a clear pest to grapevines (Boudon-Padieu et al., 2000).

CONCLUSION
Our monitoring is the first report of Halyomorpha halys in the French vineyard.This species has joined the community of Pentatomidae bugs present in these agroecosystems, at least in the Bordeaux wine production areas.The presence of nymphs in the centres of the plots show that the pest can develop in vineyard agroecosystems and pose a growing threat to wine production.Therefore, monitoring H. halys in French vineyards is important for risk assessment and, consequently, in risk management.Lionel Delbac et al.

FIGURE 1 .
FIGURE 1. Nymphs as well as an egg clutch of Halyomorpha halys on grapevine plants (Photo credit: R. Rouzes).

TABLE 1 .
Total number of Halyomorpha halys and other species of Pentatomidae recorded inside the vineyard plots and in the edges of these plots in 2018, 2019 and 2020.
N/A: data not collected; number of nymphs in brackets.