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Research Article
Two new aphid parasitoids (Hymenoptera, Braconidae, Aphidiinae) from field crops of South America
expand article infoŽeljko Tomanović§, Korana Kocić, Sofía Belén Forte|, Joel Nazareno Lentini|, María del Pilar Medialdea|, Camila Noemí Villar|, Analí Bustos|, Ana Lia Gayan-Quijano, Francisco Javier Peris-Felipo, Mariano Devoto|#
‡ University of Belgrade, Belgrade, Serbia
§ Serbian Academy of Sciences and Arts, Belgrade, Serbia
| Universidad de Buenos Aires, Buenos Aires, Argentina
¶ Syngenta Crop Protection AG, Basel, Switzerland
# Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina
Open Access

Abstract

During two seasons of field sampling in crop fields in Argentina, a total of 2,276 Aphidiinae specimens were collected using Malaise traps positioned in maize, soybean, and wheat fields. Eight known species of aphid parasitoids were identified (Aphidius platensis Brethes, 1913, A. ervi Haliday, 1834, A. rhopalosiphi de Stefani-Perez, 1902, A. uzbekistanicus Luzhetzki, 1960, A. matricariae Haliday, 1834, Diaeretiella rapae (McIntosh, 1855), Lysiphlebus testaceipes (Cresson, 1880), and Praon gallicum Starý, 1971). Additionally, two new species of aphid parasitoids were discovered, bringing the total to ten species reported from these crops in the country. Here, we describe and provide diagnoses for Aphidius brethes sp. nov. and Trioxys pampas sp. nov., which is the first record of winged species of the genus Trioxys in South America.

Keywords

A. brethes sp. nov., Argentina, Malaise trap, parasitoid wasps, T. pampas sp. nov.

Introduction

Cereal crops are among the most widespread in the world. Many different biological control programs have been used against various cereal pests, that range from fungal pathogens (Khan 2012; Newitt et al. 2019) to insect pests (Hågvar and Hofsvang 1991; Overholt et al. 1997; Starý et al. 2007; Brewer et al. 2019). Among cereal pests, aphids cause a significant decline in cereal production through direct plant damage or through the transmission and dissemination of viral pathogens (Dixon 1987; van Emden and Harrington 2017; Brewer et al. 2019). Due to their agricultural importance, aphids and their natural enemies (parasitoids and predators) are very common model systems in basic and applied research (Boivin et al. 2012). Tomanović et al. (2022) report 26 aphid parasitoid species in European cereal crops, while 12 species are known in cereals in South America (Starý 1993, 1995; Martínez-Chávez et al. 2019; Lau et al. 2023). Although there are many research efforts on the diversity and ecology of aphid parasitoids in South America (e.g. Starý 1993, 1995; Starý et al. 2007; Martínez-Chávez et al. 2019; Lau et al. 2023), in this study we additionally report, describe and diagnose two previously unknown aphid parasitoid species from crop fields in Argentina, amounting to the total number of 10 species found in these crops.

Material and methods

Systematic Aphidiinae trapping was conducted in agricultural fields within the Rolling Pampas of Argentina (Fig. 1A), a region characterized by a temperate climate (Cfa/Cfb, Köppen classification) and annual precipitation ranging from 800 to 1,200 mm. The fields followed a three-year crop rotation cycle of maize, first-crop soybean, and wheat/second-crop soybean. This study was part of a large-scale field experiment aimed at evaluating the effects of field margin management on agricultural biodiversity, including parasitoids.

Figure 1. 

A farm location in Argentina B View of a wheat field with Malaise traps’ installed within soybean field.

Initially, the study involved 12 fields, each with ten Malaise traps systematically positioned at specific distances from the field edge (10, 50, 100, and 150 meters) (Fig. 1B). Additionally, two Malaise traps were placed directly within the field margins in a 10 × 100 m strip of semi natural vegetation. One of these margin strips was experimentally manipulated by sowing selected plant species and avoiding herbicide application to promote biodiversity, while the other was left as an untreated control. Due to extreme drought and crop failures, three fields were discarded, leaving nine fields included in the final analysis.

Traps were only active during periods when crops were present in the fields. They were removed immediately prior to harvest and reinstalled a few days after sowing, with no sampling conducted during fallow periods. Trapping occurred over two years (July 2022 to April 2024). During the first year (July 2022 to May 2023), traps were continuously active and emptied twice monthly. In the second year (August 2023 to April 2024), traps operated for 15 days each month. A total of 976 samples were analyzed for Aphidiinae and other agronomically relevant arthropods. Average field size was 77.25 ha (range: 40–213 ha).

The region experiences distinct seasonal variations, with summer temperatures often exceeding 30 °C and winter temperatures dropping below freezing. The diurnal temperature range is particularly significant in summer, with average annual temperatures between 13 °C and 17 °C. Most precipitation occurs during summer months (Soriano et al. 1991; Bianchi and Cravero 2010).

Specimens were preserved in 70% alcohol and later identified to the species level. External morphology was examined using a ZEISS Discovery V8 stereomicroscope, with several specimens dissected and slide-mounted in Berlese medium. Morphological terminology follows Sharkey and Wharton (1997). All specimens are housed in the collections of the Bernardino Rivadavia Natural Sciences Argentine Museum (Buenos Aires, Argentina; MACN-En), Basel Natural History Museum (Basel, Switzerland; NMB), and the Institute of Zoology, Faculty of Biology, University of Belgrade (FBUB).

Results

In total we collected 2276 aphid parasitoid specimens, from eight species: Aphidius platensis Brethes, 1913 [866 specimens (842♀ 24♂); 38.05%], A. ervi Haliday, 1834 [731 (588♀ 143♂) (32.12%)], A. rhopalosiphi de Stefani-Perez, 1902 [2 (2♀); below 1%], A. uzbekistanicus Luzhetzki, 1960 [7 (5♀2♂); below 1%], A. matricariae Haliday, 1834 [5 (5♀); below 1%], Diaeretiella rapae (McIntosh, 1855) [621 (584♀ 37♂); 27.28%], Lysiphlebus testaceipes (Cresson, 1880) [30 (26♀4♂); 1.32%], and Praon gallicum Starý, 1971 [6 (5♀1♂); below 1%]. All collected parasitoid species are associated with pest aphids from investigated crops.

Additionally, we collected two unknown species: six specimens (5♀ 1♂) of Aphidius (Lysaphidus) sp. and two individuals of Trioxys sp. (2♀). After their examination, we found that they are new to science. Unfortunately, DNA extraction was unsuccessful, probably due to bad preservation of specimens.

Taxonomic part

Order Hymenoptera L., 1758

Family Braconidae Nees, 1811

Subfamily Aphidiinae Haliday, 1833

Aphidius brethes Tomanović & Kocić, sp. nov.

Figs 2, 3A–H, 4A–H

Type material.

Holotype : • 1 ♀, Argentina, sample 85APHI, 34°27'35"S, 61°48'46"W (Leandro N. Alem County), 29.XI.2022, collected by Malaise traps in field margin of first-crop soybean, leg. M. Devoto & collabs. Holotype deposited in coll. Museo Argentino de Ciencias Naturales ”Bernardino Rivadavia”, Argentina (MACN-En).

Paratypes : • 1 ♀, sample 540APHI, Argentina, 33°56'16"S, 59°37'04"W (Baradero County), 28.IV.2023, collected by Malaise traps in field margin of first-crop soybean, leg. M. Devoto & collabs. (MACN-En); • 1 ♀, sample 609APHI, Argentina, 34°29'22"S, 61°44'47"W (Exaltación de la Cruz County), 04.VIII.2023, collected by Malaise traps in margin of wheat field, leg. M. Devoto & collabs. (MACN-En); • 1 ♀, sample 519APHI, 34°28'56"S, 61°47'18"W (Leandro N. Alem County), Argentina, 04.V.2023, collected by Malaise traps in margin of second-crop soybean field, leg. M. Devoto & collabs. (FBUB); • 1 ♀, sample 580APHI, 33°56'16"S, 59°37'04"W (Baradero County), Argentina, 04.V.2023, collected by Malaise traps in wheat field, leg. M. Devoto & collabs. (NMB); • 1 ♂, 549APHI, 33°55'16"S, 59°37'42"W (Baradero County), Argentina, 04.VIII.2023, collected by Malaise traps in wheat field, leg. M. Devoto & collabs. (MACN-En).

Diagnosis.

By wing venation pattern (M+m-cu vein partly developed under r-m vein) (Fig. 3H) Aphidius brethes sp. nov. belongs to subgenus Lysaphidus. Aphidius brethes sp. nov. belongs to Aphidius species group with costulate anterolateral area of petiole like all known Aphidius species in South America (e.g. A. matricariae Hal., A. rhopalosiphi Luzhetzki, A. uzbekistanicus De Stefani-Perez), except for A. ervi Hal. that possesses rugose and A. avenae Hal., A. platensis Brèthes and A. colemani Viereck that have costate anterolateral area of petiole. New species differs from the mostly known Lysaphidus species by having 16–17-segmented antennae (Fig. 3B), four maxillar palpomeres and two labial palpomeres, while other species have 12–14 segmented antennae and usually three maxillar and two or one labial palpomeres (e.g. Aphidius arvensis (Starý), A. erysimi (Starý), A. adelocarinus Smith, A. rosaphidis Smith). Aphidius brethes sp. nov. by 16–17-segmented antennae and four maxillar and two labial palpomeres morphologically resembles A. viaticus (Sedlag) (15, 16-segmented antennae) and A. ramithyrus Smith (15, 16-segmented antennae). Moreover, it differs from A. viaticus on having the proportion between length and width of petiole at spiracles level 2.3–2.4 × (Fig. 3F), while A. viaticus possesses 3.0–3.5 petiole proportion. The new species differs from A. ramithyrus by shorter flagellomere 1 (proportion between length and width of F1 is 2.6–2.8 × (Fig. 3C), while in A. ramithyrus it is 3.0–3.2×) and longer petiole (2.3–2.4 × as long as width at spiracles level (Fig. 3F), while in A. ramithyrus 2.0–2.2). Furthermore, Aphidius brethes sp. nov. is mostly yellow colored (Fig. 2), while A. ramithyrus and A. viaticus are darker. Aphidius viaticus parasitizes Pleotrichophorus glandulosus (Kalt.) aphid associated with Artemisia plants, while Aphidius ramithyrus parasitize Capitophorus spp. aphids. We assume that A. brethes sp. nov. parasitizes cereal or soybean aphids.

Figure 2. 

Aphidius brethes sp. nov., habitus of the paratype female (sample ID 519APHI).

Figure 3. 

Aphidius brethes sp. nov., holotype female (sample ID 85APHI) A head B antenna C scape, pedicel, anellus, F1 and F2 flagellar segments D mesonotum E propodeum F petiole G ovipositor sheath H forewing.

Description.

Female (holotype). Length. Body 1.5–1.7 mm; fore wing 1.6 mm; hind wing 1.2 mm.

Head (Fig. 3A). Transverse, wider than mesosoma at tegulae. Eyes medium sized, oval, laterally prominent. Face moderately setose. Tentorial index (tentoriocular line/intertentorial line) 0.60–0.65. Clypeus with 8–12 long setae. Labrum distinct, with 7–8 short setae on outer margin. Malar space equal to 0.33–0.38 of longitudinal eye diameter. Mandible bidentate, with 9–10 setae on outer surface. Maxillar palpi with 4 palpomeres, labial palpi with 2 palpomeres. Antenna 16, 17-segmented, moderately thickened (Fig. 3B). Pedicel subsphaerical (Fig. 3C). First flagellomere (F1) subequal or slightly shorter than second flagellomere (F2) and 2.6–2.8 × as long as its maximum width (Fig. 3C). F1 and F2 bearing 0–1 and 2–3 longitudinal placodes, respectively (Fig. 3C). Flagellomeres covered uniformly with semi-erect setae subequal to half of segments diameter.

Mesosoma. Mesoscutum (Fig. 3D) smooth, covering pronotum from above. Notaulices not present. Mesoscutum sparsely setose with one row of setae laterally (Fig. 3D). Scutellum oval, bearing 6–7 long setae. Propodeum areolated with wide central areola, but sometimes missing upper carina (Fig. 3E). Upper and lower areolae of propodeum with 1–2 and 1–3 long setae on each side. Fore wing (Fig. 3H) densely pubescent, marginal setae longer than those on surface; pterostigma, 2.9–3.1 × as long as its width, 1.9–2.4 × as long as R1 vein (=metacarpus).

Metasoma. Petiole (Fig. 3F) elongate, dorsally striated at the middle, slightly convex dorsally; its length 2.3–2.4 × its width at spiracles, 1.8–2.0 × its width at the base (Fig. 3F); 10–12 setae positioned on dorsal posterior part; one long seta posterior to spiracles. Anterolateral area of the petiole with 10–12 costulae. Ovipositor sheath (Fig. 3G) moderately elongated, wide at base, dorsally slightly convex, narrowed toward tip, apically truncated, bearing two long setae at dorsal margin. Length of ovipositor sheath 1.6–2.0 × its maximum width at base, 2.7–3.0 × its minimum width at tip.

Coloration. General body color yellow to light brown (Fig. 2). Scapus and pedicel yellow to light brown, annellus yellow, yellow ring at the base of F1, remaining part of antennae brown. Head light brown, eyes dark. Mouthparts except tips of mandible yellow. Pronotum, mesoscutum and mesopleuron light brown. Propodeum yellow. Legs with yellow coxae and trochanters, remaining parts of legs light brown. Wings hyaline, venation yellowish brown. Petiole yellow, other metasomal terga yellow to light brown, dorsally darker. Ovipositor sheath dark brown.

Male (Figs 4A–H). Antenna 17-segmented (Fig. 4B). Maxillar palpi with 4 palpomeres, labial palpi with 2 palpomeres. Flagellomeres 1 and 2 shorter than in female, and both 1.9 × as long as wide, each bearing 7–8 longitudinal placodes (Fig. 4C). Tentorial index approx. 0.43, malar index approx. 0.63. Fore wing venation as in female (Fig. 4H). Fore wing marginal setae distinctly longer than those on surface; pterostigma widely triangular, 2.8 × as long as its width and 1.9 × as long as R1 vein (=metacarpus) (Fig. 4H). Petiole (Fig. 3F) 2.9 × its width at spiracles. Aedeagus oval (Fig. 4G) with 10–15 setae laterally. Body slightly darker than in female, head and thorax light brown, antenna brown, mouthparts yellow. Wings slightly transluscent. Legs brown with light yellow patches at ventral and tip of segments. Petiole and propodeum yellow. Coxae and trochanters yellow, remaining parts of legs light brown to brown. Metasoma light brown to brown. Body length: 1.5 mm.

Figure 4. 

Aphidius brethes sp. nov., paratype male (sample ID 549APHI) A head B antenna C scape, pedicel, anellus, F1 and F2 flagellar segments D mesonotum E propodeum F petiole G aedeagus H forewing.

Distribution.

Aphidius brethes sp. nov. was collected in Argentina and currently it is its only known distribution.

Aphid host.

Unknown, collected by Malaise traps within field crops.

Etymology.

The new species takes its name by Juan Brèthes, an Argentine scientist, naturalist, entomologist who has described several aphid parasitoid species.

Trioxys pampas Tomanović & Kocić, sp. nov.

Figs 5A–H

Type material.

Holotype : • 1 ♀, Argentina, sample 122APHI, 34°29'30"S, 61°44'39"W (Leandro N. Alem County), Argentina, 31.X.2022, collected by Malaise traps in margin of maize field, leg. M. Devoto & collabs. Holotype deposited in coll. Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”, Argentina (MACN-En).

Paratypes : • 1 ♀, 8APHI, 34°28'56"S, 61°47'18"W (Leandro N. Alem County), Argentina, 11.XI.2022, collected by Malaise traps in wheat field, leg. M. Devoto & collabs. (NMB).

Diagnosis.

The new species is distinguishable from its congeners by combination of characters: apical clawlike bristle and two short setae at the tip of prongs (Fig. 5G), propodeum carinated with irregular carinae, without central areola (Fig. 5E) and one to two and two to three longitudinal placodes on flagellomere 1 and 2, respectively (Fig. 5C). We assume that T. pampas sp. nov. parasitizes cereal aphids. It differs from T. sunnysidensis Fulbright & Pike, 2007, which attack cereal aphids in North America, Europe and New Zealand, by irregular propodeal areola (regular pentagonal in T. sunnysidensis) and by an apical clawlike bristle and two short setae at the tip of prongs (two simple bristles in T. sunnysidensis) (Fulbright et al. 2007). Trioxys pampas sp. nov. shares irregular propodeal areola and clawlike bristle on the top prongs with T. californicus Starý & Zuparko, 1995. However, it easy differentiated from T. californicus by 11-segmented antennae (T. californicus has 13-segmented antennae) and almost straight prongs (T. californicus has more curved prongs) (Fulbright et al. 2007). Additionally, T. californicus parasitizes Eucallipterus tiliae (L.) on Tilia cordata (Starý and Zuparko 1995).

Figure 5. 

Trioxys pampas sp. nov., holotype female (sample ID 122APHI) A head B antenna C scape, pedicel, anellus, F1 and F2 flagellar segments D mesonotum E propodeum F petiole G ovipositor sheath with accessory prongs H forewing.

Description.

Female (holotype). Length. Body 1.3 mm; fore wing 1.2 mm; hind wing 1.0 mm.

Head. Eye large (Fig. 5A), parallel sided, only slightly converging toward clypeus; interocular line 0.3 × of the head width; malar space approx. 0.1 of longitudinal eye diameter. Genae densely setose, remaining parts of head sparsely setose (Fig. 5A). Clypeus narrow, with 6–8 long setae. Tentorial index (tentorio-ocular line/ intertentorial line) 0.21. Malar index 0.12. Maxillary palp with 4 palpomeres, labial palp with 2 palpomeres (Fig. 5A). Mandible monodentate, bearing 6–7 long setae at outer surface. Labrum with two rows of setae with 6 setae at outer margin and three setae at inner part. Antennae (Fig. 5B) 11-segmented, moderately thickened, prevailingly with semi-erect setae which are sub-equal to the half of the segments diameter; flagellomere 1 (F1) 3.10–3.43 × as long as its median width, and with 1–2 longitudinal placodes (Fig. 5C); flagellomere 2 (F2) 2.8–3.1 × as long as its median width, with 2–3 longitudinal placodes; F1 equal to F2 (Fig. 5C).

Mesosoma. Mesoscutum with short notauli distinct anteriorly with 1–2 rows of sparse long setae at each side (Fig. 5D). Scutellum (Fig. 5D) sub-triangular, with 4 long setae at each side. Forewing: Pterostigma (Fig. 5H) triangular, 2.5–2.9 × as long as its width and 1.5–2.0 × as long as R1 vein; r & RS vein reaching to the middle of R1 vein in maximum length. Forewing surface densely covered with medium size setae and with long marginal setae (Fig. 5H). Propodeum (Fig. 5E) carinated with irregular carinae, without central areola.

Metasoma. Petiole (Fig. 5F) short, 1.6–1.7 × as long as wide at spiracles, with a pair of setae on postero-dorsal aspect, and four long lateral setae along the side. Ovipositor sheath (Fig. 5G) elongate, 3.0 × as long as its maximal width (at base); with a single long and 3–4 short setae on lateral and dorsal aspects. Prongs (Fig. 5G) almost straight and long with 3 long perpendicular dorsal setae, followed by an apical clawlike bristle and two short setae at the tip.

Coloration. Head brown, gena, face, clypeus, mouthparts light brown. Pedicel and scapus light brown to brown, annellus yellowish, flagellomere 1 and flagellomere 2 light brown, remaining part of antennae brown. Mesonotum and propodeum light brown, the rest of mesosoma yellow. Legs light brown with yellow trochanters. Petiole yellow to light brown, the rest of metasoma light brown to brown. Ovipositor sheaths and prongs light brown.

Male. Unknown.

Distribution.

Trioxys pampas sp. nov. was collected in Argentina and it is only known species distribution at the moment.

Aphid host.

Unknown, collected by Malaise traps within maize field and wheat fields margin.

Etymology.

The new species takes its name by Rolling Pampas of Argentina where was collected.

Discussion

Species composition and diversity of aphid parasitoids as important natural enemies of aphids in cereal and soybean crops are well known. The recent study on parasitoids parasitizing aphids from cereal crops in Europe reported 26 parasitoid species (Tomanović et al. 2022). Many of these species are distributed in the Palaearctic (Starý 1981; Rakhshani et al. 2008), Africa (Laamari et al. 2012), Australia (Ward et al. 2021), North America (Pike and Starý 1995; Pike et al. 2000) and South America (Starý 1993, 1995; Lau et al. 2023). The North American fauna of aphid parasitoids in cereal crops includes six species of European or Palaearctic origin (see Pike et al. 2000), but also several species that are probably native to North America: Aphidius avenaphis (Fitch, 1861), Ephedrus californicus Baker, 1909, Lysiphlebus testaceipes (Cresson, 1880), Monoctonus washingtonensis Pike & Starý, 1995, Praon occidentale Baker, 1909, P. unicum Smith, 1944 and P. yakimanum Pike & Starý, 1995. In South America, however, of the 12 known species of aphid parasitoids from cereal crops (Starý 1993, 1995; Martínez-Chávez et al. 2019; Lau et al. 2023), except for A. platensis (see Tomanović et al. 2014), all other species are introduced and not native to that region. Here, we described and diagnosed two new aphid parasitoid species from field crops in Argentina. Although we did not rear them from aphid hosts, but sampled them with the Malaise trap, we assume that both species parasitize aphids from cereals (wheat or corn) or soybean. We collected them inside field crops. We suspect that A. brethes sp. nov. and T. pampas sp. nov. originate from South America, because they have never been sampled before from any crops or non crop habitats outside this region. Aphid parasitoids of the genus Trioxys are not common in cereal crops. Starý (1981) reported T. auctus (Haliday) on the bird cherry oat aphid, Rhopalosiphum padi (L.), in Europe. Fulbright and Pike (2007) described T. sunnysidensis Fulbright & Pike from the Pacific Northwest (Washington) on the same aphid host. Later, Čkrkić et al. (2019) reported T. sunnysidensis in Europe and New Zealand. Trioxys pampas sp. nov. can be easy differentiated from North American congenerics (Fulbright et al. 2007) while A. brethes belongs to subgenus Lysaphidus, that was reviewed by Tomanović et al. (2007). Ragsdale et al. (2011) reviewed 8 North American braconid parasitoids on soybean aphids and among them no Trioxys species were found. Starý and Delfino (1986) and Starý (1995) reviewed aphid parasitoids from Tucuman Province (Argentina) and Chile, respectively and described two new Binodoxys species (originally described within genus Trioxys) – B. tucumanus Starý, 1986 and B. chilensis Starý, 1995. Subsequently, two additional Binodoxys species were reported from central Argentina, newly described B. achalensis Starý, 2004 (Delfino & Starý, 2004) and B. brevicornis (Zummofen et al. 2013). Surprisingly, T. pampas sp. nov. is the first recorded species of the genus Trioxys in South America (Yu et al. 2016) and only winged Trioxys species from crop dominated landscape in South America. Gärdenfors (1990) described T. apterus from Napo Province in Ecuador, and it was the only known Trioxys species in South America prior to our research. The distribution and biology of both newly described species in South America should be evaluated by further research, as well as their host range pattern.

Acknowledgements

We express our sincere gratitude to MSU and Adecoagro, and Santa Ines, Los Montes and La Casualidad farms for graciously permitting us to carry out this study. Additionally, our heartfelt thanks go to Julio Muriel, Hernan Barbero and Federico Pandol for their invaluable contributions to this project. The present work was funded by the project LivinGro® (Syngenta) and partially funded by the Ministry of Science, Technological Development and Innovation of the Republic of Serbia (Grant numbers 451-03-65/2024-03/ 200178 and 451-03-66/2024-03/ 200178) and the Serbian Academy of Sciences and Arts (grant no. F131).

References

  • Bianchi AR, Cravero SAC (2010) Atlas Climático Digital de la República Argentina. Ediciones Instituto Nacional de Tecnología Agropecuaria, Buenos Aires, Argentina.
  • Čkrkić J, Petrović A, Kocić K, Ye Z, Vollhardt IMG, Hebert PDN, Traugott M, Tomanović Ž (2019) Hidden in plain sight: Phylogeography of an overlooked parasitoid species Trioxys sunnysidensis Fulbright & Pike (Hymenoptera: Braconidae: Aphidiinae). Agricultural Forest Entomology 21: 299–308. https://doi.org/10.1111/afe.12334
  • Delfino MA, Starý P (2004) Uroleucon bereticum (E.E. Blanchard) (Hemiptera: Aphidiidae) and its new endemic parasitoid species (Hymenoptera: Braconidae, Aphidiinae) in Argentina. Neotropical Entomology 33(5): 577–581. https://doi.org/10.1590/S1519-566X2004000500006
  • Dixon AFG (1987) Cereal aphids as an applied problem. Agricultural Zoology Review 2: 1–57.
  • Fulbright JL, Pike KS, Stary P (2007) A key to North American species of Trioxys Haliday (Hymenoptera: Braconidae: Aphidiinae), with a summary of the geographic distribution, hosts, and species diagnostic features. Proceedings Entomological Society of Washington 109(4): 779–790.
  • Gärdenfors U (1990) Trioxys apterus sp. n. from Ecuador, a new wingless species of Aphidiinae (Hymenoptera: Braconidae). Insect Systematics & Evolution 21(1): 67–69. https://doi.org/10.1163/187631290X00049
  • Hågvar EB, Hofsvang T (1991) Aphid parasitoids (Hymenoptera, Aphidiidae): biology, host selection and use in biological control. Biocontrol News and Information 12: 13–42.
  • Khan MR (2012) Beneficial bacteria for biological control of fungal pathogens of cereals. In: In: Maheshwari D (Ed.) Bacteria in Agrobiology: Disease Management. Berlin, Heidelberg: Springer Berlin Heidelberg, 153–165. https://doi.org/10.1007/978-3-642-33639-3_8
  • Laamari M, Benferhat S, Abbes SB, Khenissa N, Chaouche ST, Halimi CW, Stary P (2012) A review of aphid parasitoids and their associations in Algeria (Hymenoptera: Braconidae: Aphidiinae; Hemiptera: Aphidoidea). African Entomology 20(1): 161–170. https://doi.org/10.4001/003.020.0119
  • Lau D, Sampaio MV, Salvadori JR, da Silva Pereira PRV, Dos Santos CDR, Engel E, Panizzi AR, Marsaro Júnior AL (2023) Historical and contemporary perspectives on the biological control of aphids on winter cereals by parasitoids in South America. Neotropical Entomology 52(2): 172–188. https://doi.org/10.1007/s13744-022-00961-0
  • Martínez-Chávez LM, Duque-Gamboa DN, Toro-Perea N (2019) New records of aphid parasitoids (Hymenoptera) from Colombia. Check List 15(6): 1083–1091.
  • Overholt WA, Ngi-Song AJ, Omwega CO, Kimani-Njogu SW, Mbapila J, Sallam MN, Ofomata V (1997) A review of the introduction and establishment of Cotesia flavipes Cameron in East Africa for biological control of cereal stemborers. International Journal of Tropical Insect Science 17(1): 79–88. https://doi.org/10.1017/S1742758400022320
  • Pike KS, Starý P (1995) New species of parasitic wasps attacking cereal aphids in the Pacific Northwest (Hymenoptera: Braconidae: Aphidiinae). Journal of the Kansas Entomological Society 68: 408–414.
  • Pike KS, Starý P, Miller T, Graf G, Allison D, Boydston L, Miller R (2000) Aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) of northwest USA. Proceedings of the Entomological Society of Washington 102: 688–740.
  • Rakhshani E, Tomanovic Z, Starý P, Talebi AA, Kavallieratos NG, Zamani AA, Stamenkovic S (2008) Distribution and diversity of wheat aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) in Iran. European Journal of Entomology 105(5): 863. https://doi.org/10.14411/eje.2008.114
  • Sharkey MJ, Wharton RA (1997) Morphology and terminology In: Wharton RA, Marsh PM, Sharkey MJ (Eds) Manual of the New World genera of the family Braconidae, 1997.
  • Soriano A, León RJC, Sala OE, Lavado R, Deregibus VA, Cauhepé MA, Scaglia OA, Velázquez CA, Lemcoff JH (1991) Río de la Plata Grasslands. In: Coupland RT (Ed.) Temperate Subhumid Grasslands, 367–407. Ecosystems of the World. 8, Natural Grasslands. Amsterdam, Elsevier.
  • Starý P (1981) Biosystematic synopsis of parasitoids on cereal aphids in the western Palaearctic (Hymenoptera: Aphidiidae, Homoptera: Aphidoidea). Acta Entomological Bohemoslov 78: 382–396.
  • Starý P (1993) The fate of released parasitoids (Hymenoptera: Braconidae, Aphidiinae) for biological control of aphids in Chile. Bulletin of Entomological Research 83(4): 633–639. https://doi.org/10.1017/S0007485300040062
  • Starý P, Delfino MA (1986) Parasitoids (Hym., Aphidiidae) of aphids (Hom., Aphidiidae) in Tucuman, Argentina. Bollettino del Laboratorio di Entomologia Agraria Filippo Silvestri, Portici 43: 41–50.
  • Starý P, Zuparko RL (1995) A new species of Trioxys (Hymenoptera: Braconidae) from California. Pan-Pacific Entomologist 71: 173–175.
  • Starý P, Sampaio MV, Bueno VHP (2007) Aphid parasitoids (Hymenoptera, Braconidae, Aphidiinae) and their associations related to biological control in Brazil. Revista Brasileira de Entomologia 51: 107–118. https://doi.org/10.1590/S0085-56262007000100018
  • Tomanović Ž, Kavallieratos NG, Ye Z, Nika EP, Petrović A, Vollhardt IM, Vorburger C (2022) Cereal aphid parasitoids in Europe (Hymenoptera: Braconidae: Aphidiinae): taxonomy, biodiversity, and ecology. Insects 13(12): 1142. https://doi.org/10.3390/insects13121142
  • Tomanović Ž, Petrović A, Mitrović M, Kavallieratos NG, Starý P, Rakhshani E, Rakhshanipour M, Popović A, Shukshuk AH, Ivanović A (2014) Molecular and morphological variability within the Aphidius colemani group with redescription of Aphidius platensis Brethes (Hymenoptera: Braconidae: Aphidiinae). Bulletin of Entomological Research 104: 552–565. https://doi.org/10.1017/S0007485314000327
  • Tomanović Ž, Rakhshani E, Starý P, Kavallieratos NG, Stanisavljević LŽ, Žikić V, Athanassiou CG (2007) Phylogenetic relationships between the genera Aphidius and Lysaphidus (Hymenoptera: Braconidae: Aphidiinae) with description of Aphidius iranicus sp. nov. The Canadian Entomologist 139(3): 297–307. https://doi.org/10.4039/n06-007
  • Ward SE, Umina PA, Macfadyen S, Hoffmann AA (2021) Hymenopteran parasitoids of aphid pests within Australian grain production landscapes. Insects 12(1): 44. https://doi.org/10.3390/insects12010044
  • Yu DS, van Achterberg C, Horstmann K (2016) Taxapad 2016, Ichneumonoidea 2015. Database on flash-drive. Nepean, Ontario, Canada. www.taxapad.com
  • Zumoffen L, Salvo A, Salto CE, Manfrino RG, Pike KS (2013) First record and redescription of Binodoxys brevicornis (Hymenoptera: Braconidae: Aphidiinae) from Argentina. Revista de la Sociedad Entomologica Argentina 72(1–2): 91–97.
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