Survey on Drosophila suzukii and Ceratitis capitata (Diptera: Drosophilidae, Tephritidae) and associated Eucoilinae species (Hymenoptera: Figitidae) in northwestern Argentina. First record of Dicerataspis grenadensis and Leptopilina boulardi as parasitoids of D. suzukii

doi:10.21203/rs.3.rs-3204055/v1

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Survey on Drosophila suzukii and Ceratitis capitata (Diptera: Drosophilidae, Tephritidae) and associated Eucoilinae species (Hymenoptera: Figitidae) in northwestern Argentina. First record of Dicerataspis grenadensis and Leptopilina boulardi as parasitoids of D. suzukii

https://doi.org/10.21203/rs.3.rs-3204055/v1

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published 16 Jan, 2024

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The Southeast Asian-native Drosophila suzukii (Matsumura) (Diptera: Drosophilidae), also known as “spotted-wing Drosophila”, is one of the most globally invasive agricultural species. Although D. suzukii is a pest spread throughout all the Argentinian fruit-growing regions, few information has been published on its impact on local fruit production. Parasitoid species associated with D. suzukii in Argentina belong to Pteromalidae (Chalcidoidea), Diapriidae (Diaprioidea), both attacking host pupae, and Figitidae (Cynipoidea), which attacks host larvae. Nine Eucoilinae (Figitidae) species, belonging to Dicerataspis, Dieucoila, Euxestophaga, Ganaspis, Hexacola and Leptopilina genera, have been associated with D. suzukii in Argentina,. Ceratitis capitata (Wiedemann), commonly known as “medfly”, is native to Africa and has a worldwide distribution, covering many tropical, subtropical and temperate regions. In Argentina, C. capitata has been associated with several native hymenopterous parasitoids belonging to Braconidae (Ichneumonioidea), Eulophidae (Chalcidoidea), Pteromalidae, Diapriidae and Figitidae families. Only two eucoline species, Ganaspis pelleranoi (Brèthes) and Rhoptromeris haywardi (Blanchard) have been related to medfly in Argentina. We report new trophic associations between the parasitoids Dicerataspis grenadensis Ashmead andLeptopilina boulardi (Barbotin, Carton and Kelner-Pillault) and D. suzukii, andbetween the parasitoid Odontosema albinerve Kieffer and C. capitata, after surveys conducted in Tucumán, northwestern Argentina. An annotated checklist and a taxonomic key of Eucoilinae associated with both invasive pests, in Argentina, is also provided.

Spotted-wing Drosophila

Mediterranean fruit fly

Fly-parasitoid associations

Larval parasitoids

Host plants Biological invasions

The Southeast Asian-native Drosophila suzukii (Matsumura) (Diptera: Drosophilidae), also known as “spotted-wing Drosophila”, is one of the most significant invasive agricultural species currently distributed in Asia, America, Europe, Africa, and even in Oceania (Garcia et al. 2022). In Argentina, D. suzukii was simultaneously found for the first time in 2014 in Río Negro on raspberry crops (Cichón et al. 2015) and in Buenos Aires on blueberry (Santadino et al. 2015). Later, it was recorded from traps placed in orange and blackberry farms in Entre Ríos (Díaz et al. 2015). During 2015, D. suzukii spread throughout much of Argentina, with captures in San Juan (de la Vega et al. 2019), in pear crops located in La Rioja (Lue et al. 2017), in cherry and berry fields in Mendoza (de la Vega et al. 2019), and in semi-arid natural habitats of Tucumán (Lavagnino et al. 2018). In 2016, D. suzukii was recorded in Tucumán infesting guava fruits and wild peach trees in a protected wildlife area, and blueberry orchards (Escobar et al. 2018; Buonocore Biancheri et al. 2022, 2023; Funes et al. 2023). It has also been collected in the provinces of Corrientes, Santa Fe and Neuquén (SENASA 2016; Gonsebatt et al. 2017; de la Vega et al. 2019). In 2017, de la Vega and Corley (2019) reported the first detection in cherry in Santa Cruz. The last records published were from the provinces of Chubut, Salta, Córdoba, Jujuy, and Misiones (Chillo et al. 2022; Socías 2022; Gandini et al. 2022). Although D. suzukii is affects Argentinian fruit crops, few information has been published about its impact on fruit production. Santadino et al. (2015) recorded a mean incidence of 59.5% of D. suzukii larvae in blueberry (Vaccinium corymbosum L.) collected from Buenos Aires. In the tropical forest of Tucumán, Escobar et al. (2018) found an incidence of 7.1% in guava (Psidium guajava L.) and Buonocore Biancheri et al. (2022) reported an incidence of 14.5% in wild peach [Prunus persica (L.) Batsch]. Later, Dettler et al. (2021) estimated a mean incidence of 9.5% in fig (Ficus carica L.) and of 61.1% in raspberry (Rubus idaeus L.) from northeast Buenos Aires. The establishment of D. suzukii in Argentina encouraged the survey of local natural enemies, such as hymenopteran parasitoids (Lue et al. 2017; Garrido et al. 2018; Funes et al. 2020; Reche et al. 2021; Gallardo et al. 2022a, b;mez Segade et al. 2022; Buonocore Biancheri et al. 2022, 2023; Funes et al. 2023). Up to date, parasitoid species associated with D. suzukii in Argentina belong to the families Pteromalidae (Chalcidoidea), Diapriidae (Diaprioidea), both attacking host pupae, and Figitidae (Cynipoidea), attacking host larvae. Figitids associated with D. suzukii belong to Eucoilinae. This subfamily is the most diverse of Figitidae from Argentina, with 53 species gathered in 23 genera all of which are solitary koinobiont endoparasitoids of Diptera Muscomorpha (Gallardo and Reche, in press). Nine eucoiline species, belonging to Dicerataspis Ashmead, Dieucoila Ashmead, Euxestophaga Gallardo, Ganaspis Förster, Hexacola Förster and Leptopilina Förster genera, have been associated with D. suzukii in Argentina (Lue et al. 2017; Funes et al. 2020; Reche et al. 2021; Gallardo et al. 2022a, b).

Ceratitis capitata (Wiedemann), commonly known as “Mediterranean fruit fly” or “medfly” is native to Africa and has a worldwide distribution, covering many tropical, subtropical and temperate regions (Copeland et al. 2002). In Argentina, it was detected for the first time in 1905 in orchards near Buenos Aires city (Vergani 1952). Later, it was reported from Concordia (Entre Ríos) in 1934 (Vera et al. 2002), from Tucumán in 1945 (Domato and Aramayo 1947) and finally it spread throughout all northeastern and northwestern regions (Vera et al. 2002) and northern Patagonia (Rial 1997). In 1994, the National Agri-Food and Animal Health and Quality Service (SENASA as per its Spanish acronym) implemented the National Fruit Fly Control and Eradication Program (ProCEM as per its Spanish acronym) to fight both the exotic C. capitata and the Neotropical-native Anastrepha fraterculus (Wiedemann) (Guillén and Sanchez 2007). According to estimations, annual losses in the Argentinian fruit production associated with direct damage by both tephritid pests vary from 15 to 20% (Guillén and Sanchez 2007). Since this national fruit fly program was established, research on medfly incidence and control has increased. Schliserman and Ovruski (2004) collected C. capitata in wild Citrus aurantium L. (sour orange) of Tucumán with a maximum infestation of 83.6 pupae/kg, while Funes et al. (2017) found C. capitata in organic orchards of blackberry (Rubus spp.) with a maximum incidence of 4,2%. Some provinces, such as San Juan and Mendoza, had used the Sterile Insect Technique as the main medfly control strategy (Díaz et al. 2008; Suárez et al. 2019). In Argentina, C. capitata was associated with several native and exotic hymenopteran parasitoids belonging to Braconidae (Ichneumonioidea), Eulophidae (Chalcidoidea), Pteromalidae, Diapriidae and Figitidae (Ovruski et al. 2003, 2006) families. However, only two eucoline species, Ganaspis pelleranoi (Brèthes) and Rhoptromeris haywardi (Blanchard) were related to the medfly (Wharton et al. 1998; Ovruski et al. 2006). Recent surveys of fruit infested by frugivorous dipterans in Tucumán revealed new records of eucoiline species associated with both invasive pests D. suzukii and C. capitata. Therefore, the objectives of the current study were (1) to report new trophic associations between two local figitid species and the invasive frugivorous dipteran D. suzukii; (2) to report the first record of Odontosema albinerve Kieffer associated with C. capitata in Tucumán; and (3) to provide an annotated checklist of eucoiline species related with both invasive fly pests in Argentina, and a taxonomic key to all the parasitoid species recorded up to date.

Study Area Description

The study site was an 800-ha-site located in a rural area at the eastern foothills of the San Javier Mountains, in the Horco Molle locality, Yerba Buena district, located at about 15 km west of San Miguel de Tucumán city Tucumán province, northwestern Argentina (Fig. 1). The area is geographically located at 26° 43ʹ 00ʺ S, 65° 22ʹ 00ʺ W, and 520–650 m altitude. The area involved the Horco Molle Flora and Fauna Experimental Reserve (REHM), the Agriculture and Saccharotechnics School (EAS), and sectors of the Sierra de San Javier Park, all of them belonging to the Universidad Nacional de Tucumán (UNT). The study site belongs to the southernmost extension of “Las Yungas” ecoregion, a subtropical montane rainforest located along the eastern slopes of the Andes Mountain range. The area is currently composed by large, deforested sectors covered by small orchards, rural housing, university facilities and patches of secondary forest with high disturbance levels, all surrounded by extensive citrus crops and large urban sectors. Climate is subtropical with a rainy-warm season from October through April, and a dry-cold season from May through September; mean annual rainfall is ca. 1450 mm and mean annual temperature is ca. 18°C (Schliserman et al. 2016).

Fruit Sampling

At a first studying phase, 140 feral peach trees, locally known as "cuaresmillo", were randomly surveyed during their peak fruiting period on each weekly sampling date from December 2014 to January 2015, December 2015 to January 2016, and December 2016 to January 2017. There were 15 collecting dates, five per surveyed period. The sample size was 40 ripe peaches per collecting date. Fruit was randomly collected from the soil beneath the tree canopy and placed into cloth bags. At a second studying phase, fallen feral peaches were also surveyed from December 2021 to March 2022. There were six collecting dates and the sample size ranged between 50 and 300 ripe peaches per sampling date. All fruit sampled were taken to the Pest Biological Control Department at the Planta Piloto de Procesos Industriales Microbiológicos (PROIMI) in San Miguel de Tucumán.

Fruit Processing

Sampled peaches were weighed, and then rinsed with a 30% sodium benzoate solution. Then fruits were placed in plastic containers (48 x 28 x 15 cm). Each container, slotted at the bottom was piled up over another plastic container of the same size. Inferior containers had unperforated bottoms covered by sterilized sand as a pupation medium. Both containers were tightly sealed with a Voile cloth lid. Both plastic containers (inferior and superior) were partitioned into sectors for individual fruit placement. Finally, they were kept in a dark room at natural environmental conditions. Sand was sifted every three days to collect fly puparia. After two weeks, each fruit was dissected in search of fly puparia remaining in the flesh or attached to the skin.

Fly Puparia Processing and Identification

All recovered tephritid and drosophilid puparia were identified by the external shape of anterior spiracles according to descriptions by White and Elson-Harris (1992) and Abram et al. (2022), respectively. Then puparia were individually processed, and transferred into 20 × 8-cm (diameter × height) plastic cups filled with sterilized moist vermiculite (Intersum®, Aislater S.R.L., Córdoba, Argentina) as pupation medium. Each cup was tightly covered with a piece of Voile cloth and held until adults emerged. The number and sex of parasitoids and flies was recorded on a weekly basis.

Adult Parasitoid and Fly Identification

M.J.B.B. identified the drosophilid flies following the keys of Takamori et al. (2006) and Vlach (2010) and the morphological description of Hauser (2011), while tephritids were identified according to Hernández-Ortiz et al. (2020). F.G., V.A.R. and L.C., identified the parasitoids using specialized bibliography (Blanchard 1947; Ovruski 1994; Reche and Gallardo 2015; Gallardo et al. 2017, 2022a, b; Reche et al. 2021) and reference insects stored in the entomological collection of the Museo de La Plata, Buenos Aires, Argentina. The flies and some adult specimens of the parasitoid were deposited in the entomological collection of the Miguel Lillo Foundation in San Miguel de Tucumán, Argentina. Most of the parasitoid specimens were deposited in the entomological collection of the Museo de La Plata (FCNyM, UNLP), Buenos Aires, Argentina.

Data Analysis

The fly relative abundance was calculated as the total number of fly puparia from each identified species over the total number of recovered fly puparia. Parasitoid relative abundance was calculated as the total number of specimens from each parasitoid species recovered from fly puparia over the total number of emerged parasitoids. Fruit infestation level was calculated as the total number of fly puparia recoverd per fruit. The parasitism percentage was estimated as the total number of emerged parasitoids over the total number of fly puparia of each identified species per 100. Spearman`s Rank-Order correlations were used to determine associations between the number of adult flies of each identified species and the number of adult parasitoids recovered from the fly species.

Checklist and taxonomic key to identification of eucoiline species

The checklist includes the following information: scientific name, synonymic list, geographical and biogeographical distributions, and hosts. Information was extracted from updated catalogs, recent publications and the present study. Species checklist follows an alphabetical order within each tribe of Eucoilinae.

Morphological terminology follows Buffington et al. (2017) and Gallardo et al. (2017, 2022a) for taxonomic characters, and Harris (1979) for surface sculpturing. Biogeographical regionalization follows the scheme proposed by Arana et al. (2017). The maps were made using the free software QGIS version 2.10.1- Pisa; the same program was used to georeference the locations of parasitoids and flies.

Fly and parasitoid relative abundance, fruit infestation levels and parasitism

From the first fruit survey phase 5,441 C. capitata puparia and 191 D. suzukii puparia were recovered from 600 collected feral peaches (~ 23 kg), which accounted for 96.4% and 3.4%, respectively, of all recovered fly puparia. Between 176 and 658 C. capitata puparia and between 28 and 51 D. suzukii puparia were recovered over 15 sampling dates at the three studying periods (Fig. 2). From those puparia, 1,855 and 107 C. capitata and D. suzukii adults, respectively, were recovered. The sex ratio was 1.3 and 0.9 female/male for C. capitata and D. suzukii, respectively. The average number of C. capitata adults recovered per period was similar, which ranged between 117 and 136 adults (Fig. 3A). On average, 22 D. suzukii adults were recovered in the third period (Fig. 3B). Fruit infestation levels for C. capitata reached averages (± SD) of 9.2 (± 2.3), 8.3 (± 1.9), and 9.7 (± 4.9) puparia per peach for the first, second and third surveying periods and 1.0 (± 0.2) puparia/peach for D. suzukii only for the third period. Parasitism on C. capitata ranged from 11.5 to 26.1% (Fig. 2) and was performed by two parasitoid species, G. pelleranoi and O. albinerve. Of the total number of parasitoid specimens obtained out of C. capitata, 937 (97%) were G. pelleranoi and 25 (3%) were O. albinerve. The sex ratio was 1.2 and 0.6 female/male for G. pelleranoi and O. albinerve, respectively. Specimens of both parasitoid species were collected during the three surveying periods (Fig. 3A). The number of recovered parasitoids was positively correlated with the number of emerged C. capitata specimens (r_s = 0.743, t(n-2) = 4.009, N = 15, P = 0.001). Parasitism on D. suzukii ranged from 0 to 3% (Fig. 2) and was caused by one specimen of D. grenadensis Ashmead and by another specimen of an unidentified Leptopilina species (Fig. 3B). The Leptopilina sp. was morphologicaly similar to L. boulardi but its identity could not be confirmed so far. There was no correlation between the number of parasitoids and the number of emerged D. suzukii adults (r_s = -0.866, t(n-2) = 3.000, N = 5, P = 0.058).

From the second fruit survey phase 15,828 C. capitata puparia and 1,841 D. suzukii puparia were recovered from 1,410 (~ 50 kg) feral peaches, which accounted for 89.6% and 10.4%, respectively, of the total fly puparia number. From C. capitata and D. suzukii puparia 5,534 and 682 adults were recovered, respectively. The sex ratio was 1.4 and 0.7 female/male for C. capitata and D. suzukii, respectively. Average (± SD) fruit infestation levels for C. capitata and D. suzukii were 11.3 (± 3.3) and 1.9 (± 1.8), respectively. Average (± SD) parasitism on C. capitata and D. suzukii was 20.2 (± 7.5) and 9.3 (± 5.4), respectively. Only G. pelleranoi was recovered from C. capitata, while L. boulardi was only recovered from D. suzukii. A total of 2,730 G. pelleranoi specimens and 190 L. boulardi specimens were identified. The sex ratio was 1.2 and 1.8 female/male for G. pelleranoi and L. boulardi, respectively.

Checklist of the Eucoilinae species associated with C. capitata and D. suzukii in Argentina

Eucoilini

Leptopilina boulardi (Barbotin, Carton and Kelner-Pillault 1979)

Cothonaspis (Cothonaspis) boulardi Barbotin, Carton and Kelner-Pillaut 1979: 20

Leptopilina boulardi; Nordlander 1980: 432

Charips mahensis; Nordlander 1980: 432

Hosts. Diptera Drosophilidae: Drosophila melanogaster (Meigen), Zaprionus indianus (Gupta) and D. suzukii (Marchiori et al. 2003; Cuch-Arguimbau et al. 2013; García Cancino et al. 2015; Wollmann et al. 2016; Knoll et al. 2017). In Argentina was associated with D. suzukii within vinegar traps in raspberries and cherries crops at Alto Valle of Río Negro and Neuquén (Garrido et al. 2018) and raspberries, cherries, blueberries, blackberries and Morus spp. at Buenos Aires province (Gallardo et al. 2022b). In the present study, this figitid parasitoid was recovered from D. suzukii puparia collected from infested wild peaches in a non-crop area of Tucumán.

Distribution. Cosmopolitan. In Argentina it is distributed throughout the provinces of Buenos Aires, Neuquén, Río Negro and Tucumán (Díaz and Gallardo 2014; Garrido et al. 2018; Gallardo et al. 2022b). This distribution belongs to the Pampean biogeografical province (Chacoan subregion), to the Patagonian biogeographical province (Patagonian subregion) and to the Yungas biogeographical province (Brazilian subregion) (Fig. 4).

Leptopilina clavipes (Hartig 1841)

Cothonaspis clavipes Hartig 1841: 357

Leptopilina clavipes; Nordlander 1980: 430

Hosts. Unknown. Found along D. suzukii in yellow pan traps and in fallen pears in Argentina (Lue et al. 2017).

Distribution. Nearctic and South American Transition Zone (Lue et al. 2016, 2017). In Argentina this species was cited for La Rioja. This distribution belongs to the Monte biogeographical province (South American Transition Zone) (Fig. 4).

Ganaspini

Dieucoila octoflagella Reche 2021

Dieucoila octoflagella Reche 2021 in Reche et al. 2021: 13

Hosts. Diptera Drosophilidae. In Argentina was obtained from D. suzukii on raspberry fruit (Reche et al. 2021).

Distribution. Neotropical (Reche et al. 2021). It has only been reported for Argentina where it is distributed throughout the provinces of Misiones and Tucumán. This distribution belongs to the Parana Forest biogeographical province (Chacoan subregion) and to the Yungas biogeographical province (Brazilian subregion) (Fig. 4).

Euxestophaga argentinensis Gallardo 2017

Euxestophaga argentinensis Gallardo 2017 in Gallardo et al. 2017: 59

Hosts. Diptera Otitidae: Euxesta eluta Loew in crops of sweet Bt corn (Gallardo et al. 2017). In Argentina was associated with D. suzukii within vinegar traps on peaches crops in Buenos Aires province (Gallardo et al. 2022b).

Distribution. Neotropical (Gallardo et al. 2017; Gallardo et al. 2022b). It has only been reported for Argentina where it is distributed throughout the provinces of Buenos Aires, Santa Fe and Tucumán. This distribution belongs to the Chaco biogeographical province (Chacoan subregion) and to the Yungas biogeographical province (Brazilian subregion) (Fig. 4).

Ganaspis brasiliensis (von Ihering 1905)

Hexamerocera brasiliensis von Ihering 1905: 12

Eucoela (Hexamerocera) brasiliensis von Ihering1914: 224

Eucoela (Hexamerocera) eobrasiliensis von Ihering 1914: 224; Borgmeier 1935: 117

Pseudeucoila (Hexamerocera) brasiliensis Borgmeier 1931: 230

Rhoptromeris brasiliensis: Nordlander 1978: 48

Ganaspis brasiliensis: Buffington and Forshage 2016: 3

Hosts. Diptera Tephritidae: species of Anastrepha such as A. acidusa (Walker), A. serpentina (Wiedemann), A. fraterculus. Diptera Drosophilidae: D.biauraria Bock and Wheeler, D. eugracilis Bock and Wheeler, D. ficusphila Kikkawa and Peng, D. lutescens Okada, D. melanogaster Meigen, D. montana Stone, D. persimilis Dobzhansky, D. pulchrella Tan, Hsu and Sheng, D. repleta Wollaston, D. rufa Kikkawa and Peng, D. simulans Sturtevant, D. striata, D. subobscura Collin, D. subpulchrella Takamori and Watabe, D. suzukii (Buffington and Forshage 2016; Daane et al. 2016; Gallardo et al. 2022a; Fellin et al. 2023). In Argentina was obtained from D. suzukii infesting raspberry fruit (Rubus idaeus L.) from Tucuman province (Gallardo et al. 2022a).

Distribution. Oriental, Neotropical and South American Transition Zone (von Ihering 1905, 1914; Borgmeier 1931, 1935; Nordlander 1978; Buffington and Forshage 2016; Daane et al. 2016; Nomano et al. 2017; Giorgini et al. 2018; Girod et al. 2018; Abram et al. 2020; González-Cabrera et al. 2020; Gallardo et al. 2022a). In Argentina it is distributed throughout the provinces of Buenos Aires, Chaco, Entre Ríos, Jujuy, Misiones and Tucumán. This distribution belongs to the Chaco, the Pampean and the Parana Forest biogeographical provinces (Chacoan subregion), to the Yungas biogeographical province (Brazilian subregion) (Neotropical region) and to the Monte biogeographical province (South American Transition Zone) (Fig. 4).

Ganaspis hookeri Crawford 1913

Ganaspis hookeri Crawford 1913: 244

Hosts. Diptera Tephritidae: Ceratitis cosyra (Walker) (Crawford 1913). In Argentina was collected along D. suzuki from yellow pan traps and from fallen pears (Lue et al. 2017).

Distribution. Neotropical and South American Transition Zone (Crawford 1913; Lue et al. 2017; Gallardo et al. 2022a). In Argentina it is distributed throughout the province of La Rioja. This distribution belongs to the Monte biogeographical province (South American transition zone) (Fig. 4).

Ganaspis pelleranoi (Brèthes, 1924)

Eucoila (Psichacra) pelleranoi Brèthes 1924: 10

Ganaspis carvalhoi Dettmer 1929: 70

Psichacra pelleranoi Weld 1952: 224

Ganaspis pelleranoi De Santis 1965: 74

Aganaspis pelleranoi Ovruski 1994: 124

Ganaspis pelleranoi Díaz et al. 2006: 273

Hosts. Diptera Tephritidae: Anastrepha antunesi (Lima), A. atrigona (Hendel), A. bahiensis (Lima), A. coronilli (Carrejo and Gonzalez), A. distincta (Greene), A. fractura (Stone), A. fraterculus, A. ludens (Loew), A. obliqua (Macquart), A. schultzi (Blanchard), A. serpentina (Wiedeman), A. striata (Schiner), A. turpiniae (Stone). Lonchaeidae: Lonchaea sp. (Guimarães et al. 2003; Ovruski et al. 2008; Garcia and Ricalde 2013; Díaz and Gallardo 2014; Garcia et al. 2020; de Sousa et al. 2021). In Argentina, Schliserman and Ovruski (2004) found it attacking C. capitata associated with C. aurantium in Tucumán province; it was associated with D. suzukii within vinegar traps in peach and raspberries crops in Buenos Aires province (Gallardo et al. 2022a, b).

In the present work, it was recovered of pupae of C. capitata on Prunus persicae.

Distribution. Neotropical and South American Transition Zone (Wharton et al. 1998; Díaz and Gallardo 2001; Díaz et al. 2006; Guimarães et al. 2003; Nuñez-Campero and Ovruski 2013; Díaz and Gallardo 2014; Gallardo et al. 2022b). In Argentina it is distributed throughout the provinces of Buenos Aires, Catamarca, Córdoba, Corrientes, Jujuy, La Rioja, Misiones, Salta and Tucumán. This distribution belongs to the Pampean, the Chaco, the Araucaria and the Parana Forest biogeographical provinces (Chacoan subregion), to the Yungas biogeographical province (Brazilian subregion) (Neotropical region) and to the Monte biogeographical province (South American Transition Zone) (Figs. 4 and 5).

Hexacola bonaerensis Reche 2015

Aporeucoela fuscipes Kieffer 1908: 131

Hexacola fuscipes Forshage et al. 2013: 241(non Hexacola fuscipes Kieffer 1907)

Hexacola bonaerensis Reche 2015 in Reche and Gallardo 2015: 81

Hosts. Diptera Ephydridae (Quinlan 1986; Reche and Gallardo 2015). In Argentina was associated with D. suzukii within vinegar traps in cherries and blackberries crops at Buenos Aires province (Gallardo et al. 2022b).

Distribution. Australian, Nearctic and Neotropical (Kieffer 1907; Quinlan 1986; Paretas-Martínez et al. 2013; Reche and Gallardo 2015; Gallardo et al. 2022b). In Argentina it is distributed throughout the province of Buenos Aires. This distribution belongs to the Pampean biogeographical province (Chacoan subregion) (Fig. 4).

Odontosema albinerve Kieffer 1909

Odontosema albinerve Kieffer 1909: 58

Odontosema anastrephae Borgmeier 1935: 113; Guimarães et al. 2005: 458

Hosts. Diptera Tephritidae: A. fraterculus, Anastrepha spp. A. striata and C. capitata. Lonchaeidae: Neosilba spp. (Borgmeier 1935; Wharton et al. 1981; Hernández-Ortiz et al. 1994; Uchoa-Fernandes et al. 2003; Nuñez Bueno et al. 2004). In Argentina, was obtained from C. capitata puparia on P. persica from Tucuman.

Distribution. Neotropical (Kieffer 1909; Borgmeier 1935; Wharton et al. 1981; Hernández-Ortiz et al. 1994; Nuñez Bueno et al. 2004; Guimarães et al. 2005; Garcia et al. 2020). In Argentina it was recorded for Misiones (Schliserman et al. 2010) and Tucumán (new record). This distribution belongs to the Parana Forest biogeographical province (Chacoan subregion) and to the Yungas biogeographical province (Brazilian subregion) (Fig. 5).

Trichoplastini

Rhoptromeris haywardi (Blanchard 1947)

Eucoila haywardi Blanchard 1947: 11

Rhoptromeris haywardi De Santis 1967: 97

Hosts. Diptera Tephritidae: A. fraterculus, Anastrepha sp., C. capitata (Turica and Mallo 1961; De Santis 1967; Garcia et al. 2020).

Distribution. Neotropical (Blanchard 1947; De Santis 1967). In Argentina is described for Entre Ríos and Tucumán. This distribution belongs to the Pampean biogeographical province (Chacoan subregion) and Yungas biogeographical province (Brazilian subregion) (Fig. 5).

Zaeucoilini

Dicerataspis grenadensis Ashmead 1896

Dicerataspis grenadensis Ashmead 1896: 744

Dissodontaspis flavipes Kieffer 1909: 59

Dicerataspis flavipes Weld 1952: 198; Gallardo et al. 2010: 25

Hosts. Diptera Tephritidae: Anastrepha amita, Anastrepha sp. and Rhagoletis sp. Drosophilidae: Zaprionus indianus (Hernández-Ortíz 1993; Wharton et al. 1998; Guimarães et al. 2000, 2004; Nunes Santos et al. 2016; Garcia et al. 2020). In Argentina, the parasitoid was recorded in association whith A. fraterculus (Wharton et al. 1998), and in the present study was obtained from D. suzukii puparia on P. persica from Tucuman province (new host).

Distribution. Neotropical (Ashmead 1896; Kieffer 1909; Weld 1952; Díaz 1974; Wharton et al. 1998; Gallardo et al. 2010). In Argentina it is distributed throughout the provinces of Misiones (Schliserman et al. 2010) and Tucumán (new record). This distribution belongs to the Parana Forest biogeographical province (Chacoan subregion) and to the Yungas biogeographical province (Brazilian subregion) (Fig. 4).

Remarks. D. grenadensis is a parasitoid of Drosophilidae and Tephritidae flies that attack a wide diversity of fruits (Hernández-Ortíz 1993; Guimarães et al. 2000). Several authors remarked a preference of this species for drosophilids more than for tephritids, pointing out that parasitoid associations with Anastrepha and Rhagoletis need to be checked (Wharton et al. 1998; Guimarães and Zucchi 2004; Guimarães et al. 2004, Gallardo et al. 2010).

Key to species of Eucoilinae associated with D. suzukii and C. capitata in Argentina

1- Dorsoposterior part of scutellum in dorsal view emarginated; antennae of female with club 6-segments, conspicuous; marginal cell open...........................................................................…….................................…..2

- Dorsoposterior part of scutellum in dorsal view rounded or bluntly rounded; antennae of female with variable number of club segments, conspicuous or inconspicuous; marginal cell open or closed......................3

2- Face with a prominent median area bounded laterally by grooves (see Fig. 1 in Gallardo et al. 2010); dorsoposterior part of scutellum in dorsal view with two small lateral angles and two conspicuous posterior angles; scutellar foveae wider than long (see Fig. 5 in Gallardo et al. 2010)............Dicerataspis grenadensis

- Face smooth (see Fig. 1 in Guimarães et al. 2005); dorsoposterior part of scutellum in dorsal view with two conspicuous posterior angles but no small lateral angles; scutellar foveae longer than wide (see Fig. 6 in Guimarães et al. 2005).….............................................................................................Odontosema albinerve

3- Mesoscutum unevenly convex with a “hump” in profile; dorsoposterior part of scutellum in dorsal view bluntly rounded (see Fig. 4 in Gallardo et al. 2017); marginal cell closed...........Euxestophaga argentinensis

-Mesoscutum evenly convex in profile; dorsoposterior part of scutellum in dorsal view rounded; marginal cell closed or open………………………………………………............................................................……...4

4- Marginal cell open; scutellum striated laterally (see Fig. 6 in Reche and Gallardo 2015)..................................................................................................................................Hexacola bonaerensis

- Marginal cell closed; scutellum areolate laterally…………………………................................…………….5

5- Body aciculate (see Fig. 1B in Reche et al. 2021); antennae of female with club 8-segments; scutellar plate with glandular pit covered by a small tooth, which in lateral view has a “snake’s open mouth” shape (see Fig. 1C in Reche et al. 2021)...................................................................................Dieucoila octoflagella

-Body smooth; antennae of female with club 6- or 7-segments; scutellar plate with setiferous punctures; glandular pit not covered by a small tooth…………………................................................................………...6

6-Scutellar plate convex; lateral depression of scutellum undefined; base of syntergum with hairy ring present, interrupted dorsally……………...………………..…………......................................................…….7

-Scutellar plate flat-shaped; lateral depression of scutellum well defined; base of syntergum with hairy ring present, as wool and complete dorsally……....…….….......................................….................................……..8

7- Antennae of female with club 8-segments. Mesoscutal hair present. Metasomal hairy ring dense (see Fig. 36 in Lue et al. 2016)……....................................................................................................Leptopilina clavipes

-Antennae of female with club 7-segments. Mesoscutal hair absent. Metasomal hairy ring scare or dense......9

8- Scutellar plate, in dorsal view, seed shape, exposing about half of scutellum. Scutellum with semi-parallel to slightly radiating ridges running the length of its dorsal surface (see Fig. 11 in Lue et al. 2016); metasomal hairy ring scarce, with few long hairs (see Fig. 12 in Lue et al. 2016)...........Leptopilina boulardi

-Scutellar plate, in dorsal view, rhombus shape, covering most of scutellum. Scutellum with dorsal surface areolate-rugose. Metasomal hairy ring dense, interrupted dorsally ……...….................Rhoptromeris haywardi

9-Antennae of female with club 6-segements, inconspicuous; dorsal surface of scutellum foveate (see Fig. 3 in Gallardo et al. 2022a); scutellar plate widest in anterior half (see Fig. 2 in Gallardo et al. 2022a)..…….………...........................................................................................................Ganaspis brasiliensis

-Antennae of female with club 7-segments, conspicuous; dorsal surface of scutellum areolate; scutellar plate subcircular………...........................................................…......................................................................…….10

10- Last three flagellomeres of female antenna very dark in color, rest of antenna much lighter in color (see Fig. 10 in Gallardo et al. 2022a); placoidal sensilla present on F7-F11; scutellar plate small and narrow, exposing most of scutellum (see Fig. 11 in Gallardo et al. 2022a)........................................Ganaspis hookeri

-Flagellomeres of female antenna all the same color throughout; placoidal sensilla present on F6–F11 or F5–F11; scutellar plate large and wide, covering most of scutellum (see Fig. 14 in Gallardo et al. 2022a)....................................................................................................................................Ganaspis pelleranoi

The knowledge of trophic relationships established between resident parasitoids and the two invasive dipteran species, D. suzukii and C. capitata, is highly relevant when implementing integrated management programs into invaded areas. In the current field study, three important findings can be highlighted as follows: (1) noticeable differences between D. suzukii and C. capitata regarding both feral peach infestation and fly parasitism rates; (2) the parasitoid O. albinerve was found for the first time associated with C. capitata in northwestern Argentina; and (3) two new trophic associations between two resident larval parasitoid species and D. suzukii were established.

The first finding remarks the relevance of feral peaches growing in non-crop environments as a suitable host plant species for the proliferation of both invasive pest species in northwestern Argentina. However, C. capitata was a predominant fly species on this host fruit because it was 7-fold more abundant than D. suzukii. This may be for two main reasons, host fruit preference and time spent in the invaded area. The peach is one of the primary C. capitata host plants added to the fact that the exotic medfly has been in the area for about 100 years (Ovruski et al. 2003, 2009). In contrast, D. suzukii preferentially attacks berries, although it is also an important pest of certain stone fruits, such as cherry (Kirschbaum et al. 2020). In addition, D. suzukii is a newly fly pest in the study area, because the first records in northwestern Argentina attacking both healthy wild guava and peach were on March 2016 (Escobar et al. 2018), and on December 2016 (Buonocore Biancheri et al. 2022). Parasitism in both fly species may follow a similar pattern. C. capitata has for a long time an assemblage of local pupal and larval parasitoids that together exert strong natural regulation of medfly populations in wilderness environments of northwestern Argentina (Ovruski et al. 2004; Schliserman et al. 2016; Buonocore Biancheri et al. 2022). Among these parasitoids, the figitid G. pelleranoi is one of the most important and frequently common medfly parasitoids as it may successfully develop inside medfly larva and emerge as an adult from the puparium (Ovruski et al. 2016; Schliserman et al. 2016; Buonocore Biancheri et al. 2022). Contrary to medfly, D. suzukii is mainly successfully attacked by resident pteromalid pupal parasitoids rather than by local figitid larval parasitoids (Buonocore Biancheri et al. 2022). Parasitism on D. suzukii by local larval parasitoids in close trophic relantionship has been very low (Reche et al. 2021; Gallardo et al. 2022a), with mean values lower than 2%, as shown by the current study. A lot of information has been published on the immune response of D. suzukii larva, which can kill parasitoid eggs laid inside it (Lynch et al. 2016). The results reveal that the immune system of D. suzukii must be playing a very important role in the lack of development of resident larval parasitoids in invaded areas (Wang et al. 2016; Rossi-Stacconi et al. 2018; Vieira et al. 2019; Yi et al. 2020; Wolf et al. 2021; Abram et al. 2022). However, only figitid larval parasitoid species native to Asia, such as G. brasiliensis, wich is a complex of cryptic species with variable host specificity (Wang et al. 2020), and Leptopilina japonica Novkovic and Kimura, have achieved high parasitism levels and high ability to thrive on this pest (Daane et al. 2016, 2021; Guerrieri et al. 2016; Mazzetto et al. 2016; Girod et al. 2018; Matsuura et al. 2018; Giorgini et al. 2019; Biondi et al. 2021; Kruitwagen et al. 2018, 2021).

With regard to the second finding, O. albinerve increases the number of Neotropical-native parasitoid species associated with the exotic C. capitata in Argentina. This figitid species was previously found in Misiones, northeastern Argentina, associated with A. fraterculus, but identified as Odontosema anastrephae Borgmeier (Schliserman et al. 2010). The distribution range of this figitid species would be apparently limited to the subtropical regions of northern Argentina. Both G. pelleranoi and O. albinerve share a similar host larval foraging behavior (Aluja et al. 2009), and forage for the same resource in the same microhabitats, fallen fruits infested with medfly larvae, in non-crop areas of Tucumán.

Interestingly, the third finding established for the first time a valid trophic relationship between L. boulardi and D. suzukii, as the figitid was directly recovered from puparia of the pest collected from fallen peaches. Previously, both insect species were captured together using vinegar traps in the provinces of Río Negro, Neuquén and Buenos Aires (Garrido et al. 2018; Gallardo et al. 2022b). However, a strong trophic relationship between phytophagous and entomophagous insects cannot be established by trap captures but obtaining the parasitoid directly from the host itself (Wharton et al. 1998). Interestingly, the figitid D. grenadensis was recoverd from D. suzukii puparia collected from peach in the study site. Wharton et al. (1998) previously recorded this parasitoid from A. fraterculus in Tucumán. D. grenadensis apparently has a wide host range, as it can successfully develop on both drosophilid and tephritid flies (Nunes Santos et al. 2016; Garcia et al. 2020).

In conclusion, despite of numerous figitid species closely associated with D. suzukii in Argentina, they do not have a relevant impact on the pest population. C. capitata, with fewer associated figitid parasitoid species, has significant parasitism rates for an invasive pest species. This parasitism is mainly caused by G. pelleranoi. Finally, the current study presented valuable tools for the correct identification of the figitid parasitoids associated with the two invasive fly pests in Argentina. The information provided in the sutudy is crucial for the development and implementation of biological control strategies against both invasive fly species. Further evaluation of resident parasitoids under laboratory conditions as potential biocontrol agent of both pest species should be considered.

Acknowledgments

We thank Patricia Colombres and Guillermo Borchia for laboratory assistance and the authorities from the Parque “Sierra de San Javier”, Reserva Experimental Horco Molle, and Escuela de Agronomía y Zacarotécnia (Universidad Nacional de Tucumán, Argentina) for allowing us to collect fruits. We thank the Comisión de Investigaciones Científicas de la Provincia de Buenos Aires (CICPBA) and Universidad Nacional de La Plata (UNLP) for their constant support.

Author Contribution

All authors conceived the research and wrote the manuscript. MJBB, LCS and SMO conducted field surveys, lab work and data analyses. VAR, LC, FEG, and MJBB identified insects. VAR, LC, FEG made the checklist and the taxonomic key. All authors read and approved the manuscript. SMO, DSK and GFRM conceptualization, funding acquisition, project administration, review and editing.

Funding Financial

National Fund for the Promotion of Science and Technology (FONCYT) from the National Agency for Scientific and Technological Promotion of Argentina (ANPCyT) (grants PICT 2017–0512, PICT 2020-01050) and Brazilian National Council for a Scientific and Technological Development (CNPq) research productivity grant (#311896/2021-9).

Declarations Conflict of Interest

The authors declare no competing interests.

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Survey on Drosophila suzukii and Ceratitis capitata (Diptera: Drosophilidae, Tephritidae) and associated Eucoilinae species (Hymenoptera: Figitidae) in northwestern Argentina. First record of Dicerataspis grenadensis and Leptopilina boulardi as parasitoids of D. suzukii

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Abstract

Figures

INTRODUCTION

MATERIAL and METHODS

Study Area Description

Fruit Sampling

Fruit Processing

Fly Puparia Processing and Identification

Adult Parasitoid and Fly Identification

Data Analysis

Checklist and taxonomic key to identification of eucoiline species

RESULTS

Fly and parasitoid relative abundance, fruit infestation levels and parasitism

Eucoilini

Ganaspini

Trichoplastini

Zaeucoilini

DISCUSSION

Declarations

References

Supplementary Files

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Journal Publication

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