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Research Article
Abundance of Japanese beetle adults and its parasitoid Istocheta aldrichi in a Quebec commercial vineyard
expand article infoJacques Lasnier, Charles-Henri de Coussergues§, Alain Baril|, Charles Vincent|
‡ Ag-Cord inc., Granby, Canada
§ Vignoble de l’Orpailleur, Dunham, Canada
| Plant Select, St-Paul-d’Abbotsford, Canada
¶ Formely Horticultural Research and Development Center, Agriculture and Agri-Food Canada, Saint-Jean-sur-Richelieu, Canada
Open Access

Abstract

Japanese beetles (Popillia japonica Newman 1841 – Coleoptera: Scarabaeidae) were detected in early 2000’s at L’Orpailleur, a commercial vineyard located in Dunham, Quebec. Canada. As their levels of damage increased significantly since 2014, a research project was conducted to document the abundance of Japanese beetle adults on foliage of vines and its parasite, the winsome fly Istocheta aldrichi (Mesnil) (Diptera: Tachinidae). From 2019 to 2023, the abundance of Japanese beetle adults was visually assessed in plots (3 × 24 m of grapevine rows) on foliage of each Vidal and Seyval Blanc cultivars. The abundance of Japanese beetle adults with at least one Istocheta aldrichi egg on their pronotum was also visually assessed. From 2019 to 2023, cages positioned near the vineyard allowed to overwinter I. aldrichi pupae to determine the first date of emergence of I. aldrichi adults. Cumulative day-degrees (>10 °C, starting April 1st) were used to report the events related to P. japonica adults, I. aldrichi, and the date of occurrence of phenological stages of grapevines (cultivar Seyval Blanc). In the monitored plots, the seasonal total number of P. japonica adults counted on Seyval Blanc foliage varied from 1955 in 2019 to 513 in 2023, while it varied from 2151 in 2019 to 496 in 2023 on Vidal foliage. From 2019 to 2023, during the period of oviposition of I. aldrichi, the seasonal average % of P. japonica adults showing at least one I. aldrichi egg on its pronotum varied from 7.6 in 2020 to 41.7% in 2023 on the cultivar Seyval Blanc, while it varied from 10.6 in 2020 to 35.5% in 2023 on the cultivar Vidal. Having discussed the agronomic context and factors involved at l’Orpailleur, we conclude that I. aldrichi had a major impact on P. japonica populations, thus providing a non-insecticidal and sustainable tactic to manage this insect.

Key Words

Biological control, Canada, grape, Istocheta aldrichi, Japanese beetle, Popillia japonica, Scarabaeidae, Tachinidae, vineyard

Introduction

The Japanese beetle (Popillia japonica Newman 1841 – Coleoptera: Scarabaeidae) was first reported outside of its native country, Japan, in a nursery of Riverton, New Jersey, USA, in 1916. It has rapidly become a serious pest of turfgrass and ornamental, horticultural and agricultural plants in the eastern USA, as vividly related by Frank (2016). The situation led to a major classical biological control program in Asia (Clausen and King 1927; Clausen et al. 1937). Clausen and King (1927) reported that nine species of parasites and one predator have been found in Japan and Chosen, i.e. three species of tachinids, two dexiids, four scoliids and one carabid. Decades later, Fleming (1968) reviewed the outcome of this program in detail.

In Canada, McLaine (1938) reported that in 1938, 26 live and 56 dead adults were found in Yarmouth, Nova Scotia; 19 and 8 dead adults were respectively found in Montreal, Quebec, and Quebec City, Quebec, in decks of cruise ships from the USA. Additionally, dead beetles were found in cars coming off Yarmouth and Toronto, Ontario. McLaine (1943) reported the first case of establishment in Canada, i.e. 32 living adults captured in Niagara Falls, On.. In Quebec in the mid-80’s, the distribution of the Japanese beetle was restricted to rosaceous ornamentals in Bedford, Qc, a municipality near Dunham, Quebec and the Quebec-Vermont border (C. Vincent, pers. obs.). Absent from a survey conducted in 1997 to 2000 in vineyards of Dunham, Qc, and Iberville, Qc, (Bostanian et al. 2003), the Japanese beetle has considerably extended its geographical distribution in Quebec since the early 2000’s. For example, Giroux et al. (2015) tested isolates of entomopathogenic Hypocreales fungi with adults collected in a tree nursery of Berthierville, Qc. It has been mentioned in various localities by Gagnon and Giroux (2019), Gagnon et al. (2023) and Legault et al. (2023). For several years, the distribution of Japanese beetle has been restricted to Eastern Canada. As of 2017, it has been detected in the False Creek area of Vancouver, B.C.. Japanese beetle is currently under directive D96-15 of the Canadian Food Inspection Agency (CFIA 2021). Brodeur et al. (2024) reviewed P. japonica with emphasis on biological control in Canada.

In Europe, Japanese beetle was found in the Azores (Portugal) in early 1970s, in the Ticino Valley Natural Park in Italy in 2014 (EPPO 2014), and in Ticino, Switzerland in 2017 (EPPO 2017). Its spread has been documented in human-dominating landscapes of Italy by Della Rocca and Milanesi (2022a) and the modeling of its spread according to land use and climate change scenarios has been documented by Della Rocca and Milanesi (2022b). Giglioli et al. (2024) developed a reaction-diffusion model to describe the spatio-temporal dynamics of P. japonica based on adult abundance data collected in Lombardy, Italy.

Wherever it establishes outside his native range, the Japanese beetle is a cause of concern because it has > 300 host plants and can form large aggregations (Potter and Held 2002). In a review documenting the imminent threat of P. japonica to Europe, Tayeh et al. (2022) listed 401 host plants, i.e. 131 main host plants and 270 secondary host plants. Typically, adults feed on foliage and larvae feed on the roots of grasses.

Owing to its important economic impact, major reviews have been published about the Japanese beetle, notably by Fleming (1968, 1972, 1976); Potter and Held (2002); EFSA (2018, 2019); Kistner-Thomas (2019), Shanovich et al. (2019), Althoff and Rice (2022), Poggi et al. (2022). Fleming (1972) provided detailed information about the biology, morphology, physiology and ecology of the Japanese beetle with data mostly gathered in the USA, where the insect is univoltine in most areas. Fleming (1972) indicated that in New Hampshire, few individuals require two years to complete their life cycle. Working in a Golf Course of Bolton, Massachusetts, Vittum (1986) reported the abundance (per m2) of eggs, larvae, pupae stages and trapped adults with pheromone plus floral scent lures, and concluded that ca. 10% of individuals required two years to complete their development. Kistner-Thomas (2019) mentioned that in southern Ontario, New Hampshire, New York, Massachusetts, New Jersey, and Pennsylvania, a portion of the population currently require two years to complete a generation.

Fleming (1976) and Potter and Held (2002) mentioned several microbial methods that have been researched to manage Japanese beetle, including bacteria, nematodes and microsporidia. Notable decrease of populations was reported in a golf course of Michigan where the microsporidia Ovavesicula popilliae caused mortality of overwintering larvae and reduced fecundity of Japanese beetle adults (Smitley et al. 2022). In the USA, O. popilliae spores have been disseminated near 11 airports in 8 regulated States (USDA 2020). Fleming (1968, 1976) and Potter and Held (2002) also discussed attempts to use predators and parasitoids in various agronomic situations in the USA.

Plants of the family Vitaceae are a preferred host of the Japanese beetle. At Hirosaki, Japan, Ando (1986) reported that the first and the last P. japonica adults are observed respectively on June 30th and July 21st on grapevines. Langford and Cory (1948) proposed a system of grape cultivar preference by adults based on four groups, i.e. from group 1 (preferred cultivars, injury very severe) to group 4 (unattractive, injury light and occasional). Amongst 32 grape cultivars compared in Kentucky, Seyval and Vidal Blanc had the highest leaf area loss (LAL) (Gu and Pomper 2008). Generally, cultivars showing an incidence of damage >70% were either European or French hybrid cultivars, and those with <70% incidence of damage were either American cultivars or American cultivars with a V. labrusca background (Gu and Pomper 2008).

When feeding on grape leaves, adult Japanese beetles typically produce various degrees of leaf area loss (Pfeiffer 2012, Fig. 1A). Although fruiting grapevines can tolerate some defoliation, severe leaf area losses will delay ripening, reduce fruit yield and quality (Boucher and Pfeiffer 1989), and possibly reduce cold hardiness. Adult feeding, notably post-veraison, at levels as low as 9–11% leaf area loss may detrimentally affect the quality of the current season’s fruit. In experiments conducted in Kentucky, where adults were controlled with insecticidal sprays from vineyard establishment through production, P. japonica defoliation of non-sprayed vines significantly reduced cluster number and yield, compared with protected vines, for all cultivars except Concord (Hammons et al. 2010).

In North America, the Japanese beetle and the Rose chafer (Macrodactylus subspinosus F. – Coleoptera: Scarabaeidae) are both gregarious species attracted to conspecifics. In some cases, large aggregations, create visually apparent infestations on suitable host plants. In non-fruiting Vitis labrusca (L.) var. ‘Niagara’, Mercader and Isaacs (2003) found that vines can tolerate foliar injury far exceeding that caused by two weeks of exposure to 40 beetles of either Japanese beetle or the Rose chafer.

Each year since 1997, weekly monitoring of arthropod pests has been done at the L’Orpailleur vineyard in Dunham, Quebec. Japanese beetle adults were detected in early 2000’s (Vincent and Lasnier 2020) and their levels of damage increased significantly since 2014 (Vincent et al. 2021). Our paper focuses on Japanese beetle as a vineyard pest in Quebec and its solitary, idiobiont and univoltine parasitoid, the winsome fly Istocheta aldrichi (Mesnil) (Diptera: Tachinidae, Fig. 1B). In Hokkaido, Japan, it is the most effective parasitoid of P. japonica (Fleming 1968). Introduced in the USA from Japan as part of a large classical biological program against the Japanese beetle (Clausen and King 1927), I. aldrichi was first released in New Jersey in 1922 (Fleming 1968). Introductions of I. aldrichi into the United States ceased in 1933 (Fleming 1968) and further work was done with established populations such that I. aldrichi has been reported in New York, Pennsylvania, New Jersey, Massachusetts, Connecticut and the District of Columbia by O’Hara and Wood (2004). In Canada it was first recorded in Nepean, On., in 2013 by O’Hara (2014, O’Hara and Wood 2024). I. aldrichi has been mentioned in various localities of Quebec by Gagnon and Giroux (2019), Lasnier et al. (2019), Legault et al. (2023), Gagnon et al. (2023) and Pelletier et al. (2023). Vincent et al. (2021) mentioned its presence, associated with P. japonica, at the l’Orpailleur vineyard in Dunham, Qc. The known host of I. aldrichi is P. japonica (Arnaud 1978). In 2023, I. aldrichi was released in Vancouver, British Columbia, where it established (Makovetski and Abram 2024).

I. aldrichi females lay one or several eggs on the pronotum of Japanese beetle adults (Fig. 1D; fig. 67 – Lasnier et al. 2019). In Japan, up to 14 eggs per Japanese beetle adult have been observed (Fleming 2008). Neonate I. aldrichi pierce a hole through the pronotum of Japanese beetle (Fleming 1968, Fig. 1E). Then, they fully develop inside their host (Fig. 1F), where they generally pupate (Fig. 1G). They overwinter in the mummified integument of Japanese beetle adults (Fig. 1H). Adults feed on aphis honeydew and at the nectar glands of various plants (Fleming 2008).

We here document the evolution of P. japonica/I. aldrichi/ system from 2019 to 2023, in the commercial vineyard L’Orpailleur located in Dunham, Quebec, Canada. We hereafter report on 1) the dates of occurrence and the abundance and their presence of Japanese beetle adults on foliage of vines and its tachinid parasitoid I. aldrichi from 2019 to 2023; and 2) the date of emergence of I. aldrichi adults, expressed as cumulative day-degrees (>10 °C, starting April 1st).

Figure 1. 

A. Damage caused to grapevine foliage by Japanese beetle adults; B. Istocheta aldrichi (Mesnil) (Diptera: Tachinidae) adult (Photo James O’Hara); C. Cage set at the L’Orpailleur vineyard to allow overwintering of I. aldrichi inside P. japonica mummies; D. P. japonica adults with one (male) and four (female) I. aldrichi eggs on their pronotum; E. Pronotum of P. japonica pierced (red arrow) by neonate I. aldrichi larva; F. I. aldrichi larva, exposed by dissection of P. japonica mummy; G. P. japonica mummy and I. aldrichi pupa; H. Dead (mummified) P. japonica adult lying on the ground with an I. aldrichi pupa inside.

Materials and methods

Located in Dunham, Quebec, Canada, L’Orpailleur is a commercial vineyard that operates on five non-contiguous sites. From 2018 to 2023, it expanded from 37 ha to 51 ha of vines in production. The main site is located at 45°07'05"N, 72°49'16"W. It includes the winery and is composed of French hybrids Vidal and Seyval Blanc grown on 24.5 ha (Fig. 2). At the main site, two methods are implemented to mitigate winter damage to vines. In main site A (13 ha), vines are hilled in the fall and unhilled in spring (see fig. 1.1, 1.2 – Vincent and Lasnier 2020). The soil between rows is harrowed three times per season. Flower strips composed of spontaneous (listed in table 2A, Vincent et al. 2021) species were established at the periphery of vine plots and Phacelia spp. sown between some rows (Vincent et al. 2021). In main site 1B (11.5 ha, Fig. 2), vines are covered with geotextiles in the fall and uncovered in spring as a second method to mitigate winter damage to vines (see fig. 1.3 – Vincent and Lasnier 2020). P. japonica were present in main sites A and B since early 2000’s and their populations increased to become of serious concern by 2014.

The monitoring scheme of P. japonica and I. aldrichi was developed in 2018 and implemented from 2019 to 2023 in the main site. Two plots highly infested with P. japonica since 2015 were selected. Each plot consisted of three adjacent 24-m rows (32 grapevines/row) of two French hybrids, namely Seyval Blanc and Vidal (Fig. 2). From mid-June to mid-October, P. japonica adults were visually monitored bi-weekly from 11h00 to 16h30, a time of day when their feeding activity is maximal (Kreuger and Potter 2001). Visual monitoring of Japanese beetle adults was done on the sunniest side of grapevines. Thus, the Seyval Blanc plot was monitored first on the south side, and the Vidal plot was monitored second on the west side. P. japonica adults exhibited thanatosis. Adults that could not be identified positively were excluded from the counts. All damage observed was on grapevine foliage. However, the importance of foliar damage was not determined because mechanical clipping of leaves was done three times per season during July and August. Leaves damaged by P. japonica feeding were shredded during these agronomic operations. Results are reported as the total seasonal counts of specimens on the three monitored rows of either Seyval Blanc or Vidal cultivars.

To determine the date of first emergence of overwintered I. aldrichi, 150 P. japonica parasitized adults (i.e., having at least one I. aldrichi egg on the pronotum) were yearly collected on grapevine foliage in July from 2019 to 2022. In the laboratory, adults were fed on fresh vine leaves until their death. From these dead individuals, 50 mummies were put in each of three fine polyester-muslin bags (ca. 90 cm long × 45 cm diameter) over ca. 7 cm of sterile sand deposited on the bottom of each bag. The mummies were covered first with 1 cm sand and second with ca. 15 cm of dried grasses and grapevines leaves. Each bag was closed with a binder clip. One bag was deposited in each of three cages positioned on a well-drained soil in the border of the vineyard. The cages (60 × 60 × 60 cm) were made with galvanized steel having 1.3 × 1.3 cm mesh-size (Fig. 1C). The covers of the cages were closed to exclude predators while allowing overwintering of I. aldrichi in near-field conditions. The following spring, the covers of the cages were removed. One-glass jar (ca. 1 L) was fitted tight to each bag and secured vertically such that emerged I. aldrichi could be visible. From 2020 to 2023, from mid-May to beginning of July, the three glass jars and the bags were bi-weekly checked to determine the date of first emergence of I. aldrichi adults.

As used by Kistner-Thomas (2019) and Vincent et al. (2021), cumulative day-degrees (>10 °C, starting April 1st) were used to report the parameters related to P. japonica adults and I. aldrichi. We also provided the date of occurrence of phenological stages of grapevines (cultivar Seyval Blanc) with the Baggiolini and Eichorn-Lorenz systems (Bloesch and Viret 2008). Meteorological data was gathered from Agrométéo Québec (2024) for the locality of Dunham according to a procedure detailed in Appendix 1. At l’Orpailleur, the risk of the last frost occurred between 20 to 30 May.

From 2018 to 2023, one spray of permethrin 38.4% E.C. (85 ml/ha) was done each year between phenological stages “Inflorescences visible” (Baggiolini = F; Eichorn-Lorenz = 12) and “Flowers separating” (Baggiolini = H; Eichorn-Lorenz = 17), i.e. 170 day-degrees >10 °C. The targeted pests were: Grape leafhopper Erythroneura comes (Say) (Cicadellidae); Tarnished plant bug Lygus lineolaris (Palisot de Beauvois) (Miridae); Grape flea beetle Altica chalybea Illiger (Chrysomelidae); and Lesser grape flea beetle Altica woodsi Isely (Chrysomelidae).

Arthropod pests were generally kept at commercially tolerable level thanks to an array of soft management tactics (e.g. flower strips) described in Vincent and Lasnier (2020) and Vincent et al. (2021). Fungal diseases were managed according to the guidelines of MAPAQ (2020).

Figure 2. 

Aerial view of main sites A and B of l’Orpailleur vineyard located in Dunham, Qc. The monitored grapevine rows (3 × 24 m) are highligthed in yellow (Seyval Blanc) and orange (Vidal). The blue arrow points North. The winery is at the lower corner at right. (Google Maps).

Results

From 2019 to 2023, adult Japanese beetles were observed on grapevine foliage of both Seyval Blanc and Vidal cultivars (Fig. 3A, B). The first observations of I. aldrichi eggs on the pronotum of P. japonica (Fig. 1D) varied from 354 (2019) to 455 (2020) day-degrees (>10 °C) and, from 2019 to 2023, oviposition ended on average at 907 and 887 day-degrees (>10 °C) on Vidal and Seyval Blanc respectively (Table 1). These observations occurred around the phenological stage “50% Fruit set” (Baggiolini = J; Eichorn-Lorenz = 27; 375 DD >10 °C) of the cultivar Seyval Blanc, i.e. 23 June to 6 July (Table 3).

From 2019 to 2023, the average last observations of I. aldrichi eggs on the pronotum of P. japonica occurred at 852 (Seyval Blanc) and 993 (Vidal) day-degrees (>10 °C) (Table 1). These observations occurred slightly before the phenological stage “Veraison beginning” (Baggiolini = M; Eichorn-Lorenz = 35; 900 DD >10 °C) of the cultivar Seyval Blanc, i.e. 9 to 21 August (Table 3).

From 2019 to 2023, the average seasonal of P. japonica adults showing at least one I. aldrichi egg on its pronotum varied from 7.6 (2020) to 41.7% (2023) on the cultivar Seyval Blanc, while it varied from 10.6 (2020) to 35.5% (2023) on the cultivar Vidal.

In monitored plots (Fig. 2), the seasonal total number of P. japonica adults counted on Seyval Blanc foliage varied from 1955 (2019) to 513 (2023), while it varied from 2151 (2019) to 496 (2023) on Vidal (Fig. 4).

In the three overwintering cages (Fig. 1C), the first emergence of overwintered I. aldrichi adults occurred, on average, on 285, 263 and 269 day-degrees (>10 °C) (Table 2). The earliest emergences occurred on 274, 240, 253 and 253 day-degrees (>10 °C) respectively in 2020, 2021, 2022 and 2023. These observations occurred slightly before the phenological stage “50% flowering” (Baggiolini = I; Eichorn-Lorenz = 23; 315 DD >10 °C) of the cultivar Seyval Blanc, i.e. 20 June to 2 July in calendar dates (Table 3).

Table 1.

Day-degrees (>10 °C) corresponding to the first and last (in parentheses) observation of adults P. japonica parasitized on foliage of Seyval Blanc and Vidal cultivars.

Cultivar 2019 2020 2021 2022 2023 Average
Seyval Blanc 354 (916) 455 (993) 397 (852) 401 (884) 384 (891) 398 (907)
Vidal 354 (883) 455 (900) 397 (852) 401 (910) 384 (891) 398 (887)
Figure 3. 

Percent of Japanese beetle adults having at least one I. aldrichi egg on their pronotum as a function of degree-days (> 10 °C). Counts were made from 2019 to 2023 on: A. Seyval Blanc; and B. Vidal foliage.

Table 2.

Day-degrees (>10 °C) corresponding to the first emergence, from 2020 to 2023, of overwintered I. aldrichi adults in three cages positioned in the l’Orpailleur vineyard.

2020 2021 2022 2023 Average
Cage 1 324 273 288 253 285
Cage 2 274 273 253 253 263
Cage 3 274 240 288 273 269
Table 3.

Date of occurrence of phenological stages of grapevines of cultivar Seyval Blanc grown at the l’Orpailleur vineyard (Dunham, Qc) from 2019 to 2023. (Data of 2019 and 2020 are reproduced from Vincent et al. 2021).

Phenological stage (Baggiolini Eichhorn-Lorenz)* Day degrees (>10 °C) starting April 1st 2019 2020 2021 2022 2023
Woolly bud (B 03) 25 10 May 19 May 11 April 09 May 15 April
Bud swell (C 05) 48 23 may 21 May 13 May 12 May 22 April
Green shoot (D 06) 56 25 may 23 May 15 May 13 May 05 May
2 to 3 leaves unfolded (E 09) 75 30 May 26 May 18 May 14 May 12 May
Inflorescences clearly visible (F 12) 125 10 June 29 May 22 May 22 May 28 May
Single flowers in compact groups (G 15) 145 13 June 04 June 25 May 26 May 31 May
Flowers separating (H 17) 170 17 June 06 June 02 June 29 May 01 June
50% Flowering (I 23) 315 02 July 22 June 20 June 19 June 23 June
50% Fruit set (J 27) 375 06 July 27 June 23 June 26 June 28 June
Veraison beginning (M 35) 900 21 Aug 09 Aug 12 Aug 14 Aug 15 Aug
Beginning of harvest (N 38) 17 Sept 7 Sept 09 Sept 10 Sept 11 Sept
Day Degrees (>10 °C) at beginning of harvest 1 072 1 184 1 203 1 160 1 151
No. Days between Woolly bud (B 03) and beginning of harvest (N 38) 129 110 150 124 149

Discussion and conclusion

From 2020 to 2023, the first emergence of I. aldrichi adults preceded that of observations of P. japonica adults on foliage by 154 day-degrees (>10 °C) on average, i.e., 17 days under climatic conditions prevailing at l’Orpailleur.

From 2019 to 2023 in the monitored plots (Seyval Blanc and Vidal cultivars), the seasonal total number of Japanese beetle adults generally declined (Fig. 4), while the average seasonal % of Japanese beetle adults showing at least on egg on their pronotum inversely increased (Fig. 5).

Figure 4. 

Seasonal total number of P. japonica adults counted in monitored plots (Seyval Blanc and Vidal cultivars) from 2019 to 2023.

Figure 5. 

Seasonal average % P. japonica adults showing at least one I. aldrichi egg on their pronotum counted in monitored plots (Seyval Blanc and Vidal cultivars) during oviposition period of I. aldrichi from 2019 to 2023.

It is noteworthy that, from 2018 to 2023, the only insecticidal treatment was done at the phenological stage “Flowers separating” (H 17), while the first emergence of overwintered I. aldrichi adults occurred at the phenological stage “50% flowering stage” (I 23). There was, on average, 145 DD (>10 °C) between these two events, i.e. about 17 calendar days. Under these conditions, first emerged I. aldrichi adults were likely not exposed to insecticidal residues that could have lethal or sub-lethal effects. This is supported by the fact that I. aldrichi eggs were observed on the pronotum of P. japonica adults, albeit at variable levels, throughout the period encompassed between 354 (2019) and 993 (2021) (DD>10 °C) (Table 1).

Overall, the abundance of Japanese beetle adults in the monitored plots (Fig. 2) reflected that of the main sites A and B at l’Orpailleur such that, from 2018 to 2023, no insecticidal treatment was required against P. japonica. Management of arthropod biodiversity of the vineyard with flowering strips (Lasnier et al. 2019; Vincent and Lasnier 2021) positioned near the borders was also a contributing factor allowing refuge and food resources for natural enemies nearby grapevines, and thus production of grapes with minimal insecticidal input. Basically, the agronomic and protection program changed little at l’Orpailleur from 2018 to 2023. At the vineyard l’Orpailleur, from the first detection of Japanese beetles in early 2000’s (Vincent and Lasnier 2020) to the first observation of I. aldrichi in 2015 (Vincent et al. 2021) about a decade have elapsed. Under the favorable conditions experienced at l’Orpailleur, it took I. aldrichi about 9 years to achieve biocontrol of Japanese beetle.

As the development of the crop also modifies the number of eggs deposited (Fleming 1976), considerations about soil management are in order. In contrast to golf courses (e.g. Vittum 1986) where dense gramineae offers numerous small roots over large surfaces, vineyards offer a less favorable habitat for P. japonica females to lay eggs. At main site A of l’Orpailleur, vines are mechanically hilled at the beginning of November to mitigate winter damage to vines (Vincent et al. 2021). The vines are unhilled in late April – beginning of May. In summer, three mechanical weeding were done between vine rows. Thus, the soil between vine rows is devoid of cover crops most of the time. Mechanical disturbance is such that egg laying of females is likely relatively low between rows of vines and egg survival is low. As these operations were done each year from 1997 to 2023, one cannot conclude that they were major factors explaining the rise and fall of Japanese beetle populations. P. japonica adults associated with eggs laid in soil of the flower strips and fallow plots at the periphery of vines had a higher likelihood of encountering I. aldrichi adults which could feed on floral resources. In 20 vineyards of Wisconsin, Henden and Guédot (2022) observed that higher P. japonica populations and greater leaf injury were found at vineyard edges. The proportion of pastures in the surrounding landscape, and temperature best explained the variability in P. japonica adult populations, while location, temperature, and pesticide usage (expressed as Environmental Impact Quotient) best explained variability in leaf injury Henden and Guédot (2022).

In contrast to Fleming (1968) who stated that, in Hokkaido, Japan, I. aldrichi is well synchronized with P. japonica, Pfeiffer (2012) stated that, in Virginia, USA, I. aldrichi is not well synchronized with P. japonica and only attacks the earliest-emerging adults, missing the peak of P. japonica activity. Climatic conditions experienced in Hokkaido are closer to those experienced in Dunham, Qc, than in Virginia. Thus, in the Köppen-Geiger classification of climates (Beck et alk. 2018), Southern Quebec is classified as Dfb (Snow fully humid warm summer); Hokkaido is dominated by Dfb (Warm humid continental climate), and, to a lesser extent, Dfa (Hot humid continental climate); and Virginia is Cfb (Warm temperature fully humid with warm summer). In winter, Southern Quebec and Hokkaido have a snow cover, while snow cover is rare in Virginia. In northern Japan, I. aldrichi parasitized 30–35% of P. japonica females in years of high beetle abundance, and up to 100% in years of low P. japonica abundance (Clausen 1977).

From the first observation of Japanese beetle in North America to a decline of Japanese beetle of its populations caused by I. aldrichi in a commercial vineyard of Dunham, Quebec, several decades have elapsed. Here is the timeline of entomological events that unfolded. In the USA: 1) the first observation of P. japonica in Riverton, N.J., in 1916; 2) as part of massive classical biological program conducted in Asia by USDA, I. aldrichi was first released in New Jersey in 1922 and released for 30 years in several States (Fleming 1968); 3) I. aldrichi has established in Eastern USA from New York and Massachusetts to the District of Columbia but is absent from Michigan (Fleming 1968; Cappaert and Smitley 2002). In Canada, 1) first establishment of P. japonica in Niagara Falls, Ontario (McLaine 1943); 2) First mention of I. aldrichi in Nepean, Ontario, in 2013 by O’Hara (2014). In Quebec, weekly monitoring of the l’Orpailleur vineyard from 1997 to 2023 provided a long term perspective and allowed to document major entomological events pertaining to the P. japonica/I. aldrichi system as they unfolded, i.e.: 1) in early 2000’s, first observation of P. japonica adults on cultivated vines; 2) 2014, levels of foliar damage by P. japonica adults increased significantly in main sites A and B, causing concern of using border and localized treatment synthetic insecticides post-flowering to maintain foliar damage at economically tolerable levels; 3) 2015, first observation of I. aldrichi eggs on the pronotum of P. japonica adults (Vincent et al. 2021); 4) 2023 – major decrease of P. japonica populations effected by I. aldrichi parasitism in main sites A and B.

A viticultural series of events unfolded at the vineyard L’Orpailleur in Dunham, Quebec: 1) from 1997 to 2023, L’Orpailleur has been committed to implement an array of practices that favoured conservation biological control and sustainable viticulture; 2) from 2014, implementation of flower strips in peripheral areas of main sites A and B provided refuge and food resources to I. aldrichi as well as other natural enemies, notably Anystis baccarum (Anystidae), Toxomerus spp. (Syrphidae), Therion spp. (Ichneumonidae), Nabis americoferus (Nabidae), Zelus luridus (Reduviidae). For more examples see Lasnier et al. (2019, p. 79–102) and Vincent and Lasnier (2020 – fig. 2). These strips were minimally managed and unsprayed with pesticides; 3) low usage of insecticides in the vineyard, i.e. one treatment per year between phenological stages “Inflorescences visible” and “Flowers separating”, i.e. 170 day-degrees >10 °C.

On Seyval Blanc grown in Virginia, Boucher and Pfeiffer (1989) concluded that the failure of naturally occurring populations of adult P. japonica to produce significant effects on fruit quality or quantity suggests that P. japonica may not be an economic problem on grapevines in all years, and that repeated insecticide sprays may not always be warranted. Although the biocontrol success here reported was not deliberately planned, the favorable conditions provided over a long period at l’Orpailleur allowed to meet the challenge of sustainable viticulture (Daane et al. 2018). Looking forward, the challenge for l’Orpailleur is to maintain a protection program with the least use of synthetic pesticides, notably insecticides.

Acknowledgements

We thank Alain Bazinet, Alexis Boily and Jérémie Côté for technical support. We thank James O’Hara for confirmation of the identification of specimens of I. aldrichi and for photo 1B. Otherwise stated, all photos were taken by J. Lasnier.

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Appendix 1

As mentionned in the Materials and Methods section, day-degrees (>10 °C) were calculated as follows:

  1. access https://www.agrometeo.org/
  2. Select a language (French or English) in the upper right corner. Here we selected English.
  3. Click on “AgWeather”
  4. On the left, click on “General”
  5. In center-right box, scroll down to “Summaries and forecasts”.
  6. In the first row, click on “Daily ?”
  7. On the right side, under “1. Date selection”, fill the two boxes with a starting and an end date. For example, here we put «1 April 2022» and «31 October 2022».
  8. On the right side, under “2. Base T° selection”, fill the box with a base temperature. Here we put «10». Then, click “Get summary”
  9. On the right side, click “3. Station selection”. At right under «Enter your zip code, city or the name of a station to display the corresponding stations», select a Station by scolling down blue items on the menu. Here we selected «Dunham».
  10. On the lower right, click on “Get summary”.
  11. A Table showing «Date, Avg T° (°C), Min T° (°C), Max T° (°C), Rainfall (mm), Rainfall April 1 st (mm), Dd10, Dd April 1 st» will be generated.
  12. By clicking on the upper right button “Print”, you can get a paper or a pdf copy of the Summary Table.
  13. Repeat the above procedure for the desired period and year

(This procedure was validated on 15 February 2024).

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