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. 2024 Mar 16;24(2):10. doi: 10.1093/jisesa/ieae032

New records of three parasitoids, Pteroptrix chinensis, Aphytis hispanicus, and Marlattiella prima (Hymenoptera: Aphelinidae) associated with an exotic scale, Lopholeucaspis japonica (Hemiptera: Diaspididae) in Tennessee

Johnson Alfred Daniel 1, James B Woolley 2, Karla M Addesso 3,✉
Editor: Norman Leppla
PMCID: PMC10944014  PMID: 38491949

Abstract

A survey for parasitoids of Lopholeucaspis japonica Cockerell (Hemiptera: Diaspididae), an exotic scale of woody ornamentals, resulted in the discovery of 3 species of aphelinid parasitoid wasps, Pteroptrix chinensis (Howard), Aphytis hispanicus (Mercet), and Marlattiella prima Howard. This serves as the first report of these parasitoids reared from a host in the state of Tennessee, USA. Despite routine pesticide applications in the surveyed nursery and directed treatments of the infested plants to control the scale outbreak, the percentage of parasitized scale in privet and euonymus shrubs averaged 7.0% and 7.9%, respectively. These parasitoids may be useful in the natural or managed control of this pest in the United States, but additional research is needed to understand how these parasitoids contribute to the control of L. japonica in the landscape and how nursery production practices can be modified to promote parasitoid populations.

Keywords: non-native, Japanese maple scale, Diaspididae, parasitoids, Aphelinidae

Introduction

The non-native Lopholeucaspis japonica (Cockerell) is an armored scale in the family Diaspididae (Hemiptera). It is reported as a serious pest throughout Asia, Eastern Europe, and South America (EPPO 2016). It was first reported in the United States in Connecticut in 1914 (Miller et al. 2005). Currently, the distribution range of this scale in the United States includes Alabama, Connecticut, Delaware, Georgia, Indiana, Kansas, Kentucky, Louisiana, Maryland, Missouri, Nebraska, New Jersey, New York, North Carolina, Ohio, Pennsylvania, Rhode Island, Tennessee, Texas Virginia, and Washington DC (Frank et al. 2013, García Morales et al. 2016, Jeger et al. 2018, Gilder et al. 2020). It has a host range of approximately 97 plant species from 35 families (Miller and Davidson 2005, Harsur et al. 2018, Jeger et al. 2018, Shrewsbury et al. 2020).

In the eastern United States, this scale insect has been identified as a nursery pest in woody ornamental production regions (Fulcher and Halcomb 2012, Addesso et al. 2016). There were at least 26 recorded shipment rejections of nursery trees from Tennessee in the last 3 years due to its infestation, posing an economic threat to growers and a hit to the nursery industry’s reputation (pers. comm, Tennessee Plant Certification Administrator). The survival strategies of this scale include a wide host range, small size, waxy armored covering, and cryptic coloration. The wax repels water and therefore is effective at protecting scales from insecticide formulations applied in water and also acts as a barrier against generalist predators. These features make L. japonica challenging to manage. Only adult males and crawlers are mobile and the crawler stage is the most vulnerable stage to predators and insecticides. The crawlers of this scale, however, are reported to secrete their wax covering within a few short hours after settling (Gill et al. 2014) which minimizes the amount of time they are vulnerable. Moreover, this scale feeds primarily on bark tissue, not leaves, which further complicates management as bark feeding can also reduce the efficacy of systemic insecticide treatments against scales (Addesso and O’Neal 2018). The combined attributes of this scale necessitate a multifaceted approach to management, including the use of natural enemies that can overcome the physical and physiological adaptations of this pest.

While outbreaks of this scale have become common in nursery production, population levels do not appear as high in adjacent woods (pers obs.) which led us to hypothesize that scale populations are controlled at the landscape level by natural enemies. We currently know very little about the identity of natural enemies of this scale in landscape or nursery production or how much they contribute to population control. To date, Marlatiella prima Howard, an exotic parasitoid wasp native of China and Japan, is the only reported parasitoid in the United States for this pest (Krombein et al. 1979, Gilder et al. 2020). In this context, we surveyed a woody ornamental production nursery infested by this scale with the goal of recovering parasitoids in the middle Tennessee region.

Materials and Methods

We surveyed a nursery in middle Tennessee (35.5574°N, −85.9091°W, Warren County, Morrison, TN) in late June 2023. Scale-infested plant shoots approximately 15 cm long with 1 cm diameter were collected from burning bush (Euonymus alatus [Thunb.]) and Chinese privet (Lingustrum sinense Lour.). We collected infested shoot samples from 7 privet and 20 euonymus plants grown in 5-gallon containers. The samples were brought back to the lab for evaluation. The total number of scale covers on each shoot section was counted, as well as the number of parasitoid exit holes on each shoot. We determined the percent parasitization of each sample by dividing the number of emergence holes by the total number of scales. Upon confirming the presence of parasitoids at the nursery, we collected additional material in early July 2023 to identify the number and species diversity of the parasitoids present. We collected 26 privet samples and 9 euonymus samples and held them in plastic emergence vials at room temperature. We observed each vial and assessed parasitoid emergence daily for 20 days. The emerged parasitoids were preserved in absolute alcohol and were counted using a stereo microscope (Zeiss Stemi 2000-C, Leica Microsystems, Wetzlar, Germany). Specimens were critical-point-dried at Texas A&M (Gordh and Hall 1979) and card-mounted or slide-mounted in Canada balsam using the methods described in Noyes (1982). Specimens were identified using the keys in Gibson et al. (1997), Rosen and DeBach (1979), and by comparing them with identified specimens in the Texas A&M University Insect Collection (TAMUIC). Voucher specimens have been deposited in TAMUIC under voucher number 761. Morphological terminology below follows (Gibson et al. 1997). Imaging was done using 10× and 20× Mitutoyo Plan-Apochromat objectives mounted in a Macropod system (see macroscopicsolutions.com) and an Olympus BH2 compound microscope equipped with Plan-Apochromat objectives and a Canon EOS 5D camera connected to a Windows 10 computer running Promicra QuickPHOTO software. Focus-stacking was performed in ZereneStacker Version 1.04 and contrast enhancement and minor color correction of images was performed in Adobe Lightroom Version 13.0.1.

Results

Parasitism levels averaging 7.0% were observed in infested privet plant samples and 7.9% in the euonymus samples (Table 1). The range of parasitism among the replicates was 3.8–11.5% for privet, and 0.7–34.3% for the euonymous samples. Three species of parasitoids belonging to the family Aphelinidae were recorded in this study: Pteroptrix chinensis (Howard) (Fig. 1), Aphytis hispanicus (Mercet) (Fig. 2), and Marlattiella prima Howard (Fig. 3).

Table 1.

Percent parasitism and parasitoid emergence from privet and euonymus samples

Plants Scales
(mean ± SEM)		 Emergence holes
(mean ± SEM)		 % Parasitism
(mean ± SEM)		 Parasitoids Total
Privet 294 ± 50 18 ± 3 7.0 ± 1.2 Pteroptrix chinensis 94
Marlattiella prima 29
Aphytis hispanicus 11
Euonymous 460 ± 68 29 ± 4 7.9 ± 1.7 Pteroptrix chinensis 14
Marlattiella prima 11
Aphytis hispanicus 9
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Fig. 1.

Fig. 1.

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Pteroptrix chinensis (Howard) female: a) dorsal habitus; b) head and antennae; and c) fore wing.

Fig. 2.

Fig. 2.

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Aphytis hispanicus (Mercet) female: a) dorsal habitus; b) head and antennae; and c) fore wing (lc = linea calva).

Fig. 3.

Fig. 3.

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Marlattiella prima (Howard) female: a) dorsal habitus; b) head and antennae; and c) fore wing (anl = anellus, lc = linea calva).

A total of 94 Pteroptrix chinensis emerged from the infested privet samples followed by 29 M. prima and 11 A. hispanicus (Table 1). A similar trend was observed in the case of euonymus samples, with P. chinensis being the most dominant (14) followed by M. prima (11) and A. hispanicus (9) being the least numerous (Table 1).

Discussion

Pteroptrix species closely resemble those of the genus Encarsia but can be differentiated by their 4-segmented tarsi. Our specimens of P. chinensis (Fig. 1a–c) agree well with the drawings in Xu and Huang (2004) and with a long series in TAMUIC of P. chinensis collected in Japan on Aulacaspis rosae Bouché and determined by A. B. Gahan. However, Luke Kresslein (USDA, Systematic Entomology Laboratory, National Museum of Natural History, Washington D.C., USA) noted that our specimens appear to differ slightly in antennal proportions from the type material that he examined at the National Museum of Natural History.

Pteroptrix chinensis is a parasitoid of the California red scale (Aonidiella aurantia [Maskell]) on citrus in South China, and it has been regarded as a potential control of the California red scale in California since its discovery in 1906 (Flanders et al. 1958). Currently, it is distributed in countries including India, Italy, Japan, China, Russia, Taiwan, Hawaii, and California of the United States (UCD Curators 2023). It is also known to parasitize L. japonica in Japan (Japoshvili et al. 2013). Our current study serves as a range extension in the United States for this parasitoid.

Aphytis hispanicus (Fig. 2a–c) can be identified with the following sets of characters mentioned in Abd‐Rabou (2004) and Rosen and Debach (1979). Like other members of the proclia species group, A. hispanicus has an occiput with a fuscous to black bar on each side of the foramen, but in hispanicus this is particularly well marked. The gaster is not uniformly fuscous dorsally, but paler with short fuscous strips on sides, and at most, with complete cross-bands on terga 1–5 (Fig. 2a). The pedicel and flagellum are uniformly fuscous and the apex of club is blackish (Fig. 2b). It is perhaps most similar to Aphytis comperei DeBach and Rosen, but it can be distinguished from this species using the characters and diagnosis in Rosen and DeBach (1979).

A. hispanicus is a south Palearctic species that is now widespread in the northern hemisphere. It has been reared from scale insects such as Parlatoria pergandii Comstock in Israel, Turkey, Trinidad, Brazil, Mexico, Texas, and California, from Parlatoria cinerea Doane and Hadden in Trinidad, from Chrysomphalus dictyospermi (Morgan) and Acutaspis scutiformis (Cockerell) in Brazil, from California red scale material (probably chaff scale) in Morocco, and from undetermined hosts in Italy, Jamaica, Taiwan, and Florida. Yasnosh (1972) recorded A. hispanicus as a parasite of P. pergandii, P.oleae (Colvee), Aspidiotus nerii Bouche, Lopholeucaspis japonica (Cockerell), Mytilaspis conchiformis (Gmelin) [=Lepidosaphes ficus (Signoret)], and Insulaspis pallida (Green) in the Caucasus. Populations of A. hispanicus are commonly uniparental (thelytokous) and the species often occurs in sympatry with Aphytis comperei DeBach and Rosen (Woolley and Browning 1987). Yasnosh (1978) noted that introductions of A. hispanicus were in progress along the Black Sea coast of the Caucasus, but she provides no further details. Gerson (1967) reported parasitism rates of 4% to almost 30% by A. hispanicus on P. pergandii in 2 A. hispanicus locations in Israel.

Marlattiella prima (Fig. 3a–c) was identified by comparison with specimens collected in Texas during the study of Gilder et al. (2020). This material had been compared with the type material of M. prima in the NMNH. The genus Marlattiella is a distinctive member of the subfamily Aphelininae (Kim and Heraty 2012), generally characterized by a linea calva in the forewing (lc: Figs. 2c and 3c) and 3 funicle segments and an unsegmented clava in the antenna (Fig. 2b). However, Marlattiella spp. individuals can be differentiated from other Aphelininae by a single anellus in females (transverse funicular, anl: Fig. 3b), no anellus in males, i.e., the antenna is 3-segmented in males, Tachikawa (1962a), and a long clava in the antenna. Some species of Aphytis share this antennal formula but unlike Marlattiella, Aphytis species have a longer propodeum that bears marginal crenulae on the posterior margin (Rosen and DeBach 1970). Eretmocerus species have a similar antennal formula, but the tarsal formula is 4-4-4 (Kim and Heraty 2012). M. prima is originally a native of China and Japan and it is known to parasitize L. japonica (UCD curators, 2023). In the United States, M. prima was reported in 1979 in Maryland and in 2020 in Texas (Krombein et al. 1979, Gilder et al. 2020). Suh and Evans (2019) and Xu and Huang (2004) mention this species as attacking L. japonica in Korea and China, respectively, but neither provide information on its potential impact.

Although Pteroptrix chinensis and Aphytis hispanicus have been previously reported as parasitoids of L. japonica, the current study establishes them as parasitoids of this pest in the United States for the first time. The biology of these parasitoids may contribute to their ability to disperse and establish outside their native range. Some populations of Aphytis hispanicus have been reported as uniparental (thelytokous), with populations that do not require a male for reproduction. In our survey, we only reared out female A. hispanicus. If the population in Tennessee is thelytokous, this could greatly facilitate the establishment in new areas. Further collections of the species are required to confirm whether males are present in the population. Pteroptrix chinensis is a heteronomous hyperparasitoid (Hunter and Woolley 2001), meaning males are parasitic on conspecific females or on females of other species. Although some have suggested that this life history may lead to failures in colonization efforts in new habitats (Flanders et al. 1958, Rosen and DeBach 1970), many species of heteronomous hyperparasitoid Encarsia have been used successfully in biological control programs (Zang et al. 2011).

Due to the severity of the L. japonica infestation, the grower treated both plant container species with pesticides before our survey. The parasitization percentages of 7.0 and 7.9 from privet and euonymus samples were surprisingly high, despite the routine and targeted pesticide sprays in the surveyed nursery. These wasps could have some degree of resistance to the insecticides used by the grower and/or were not present as adults during application periods. Prior studies report that the adults of A. hispanicus can emerge from underneath the waxy secretions of the scale insect without making an exit hole (Gerson 1967, 1968, Rosen and DeBach 1979). Consequently, parasitization levels could be even higher in the field since we used the exit holes to calculate the percentages.

Our study represents the first occurrence of these 3 parasitoids, Pteroptrix chinensis, Aphytis hispanicus, and Marlattiella prima in Tennessee. This record expands the distribution range of the parasitoids to the southeastern region of the United States, having previously been recorded only from the western United States, California (P. chinensis) and the northeastern region of Maryland and the central region of Texas (M. prima). Additional surveys are planned to create a comprehensive list of parasitoids of L. japonica in Tennessee. Further studies of these parasitoids related to their parasitic potential and conservation will aid us in improving the management of L. japonica by promoting their natural enemies.

Acknowledgments

We thank Andrew Polaszek from the Natural History Museum, London, UK, and Luke Kresslein from USDA, Systematic Entomology Laboratory, National Museum of Natural History, Washington D.C., USA, for assistance in confirming the identity of our specimens. We also thank Paul O’Neal, Angelo Woods, and Cheyenne Morales for assistance in collecting the parasitoids. Our special thanks to the nursery owner for allowing us to collect the samples. This project was funded by the United States Department of Agriculture (USDA)-National Institute of Food and Agriculture (NIFA)-Evans Allen (TENX 2131-CCOCP).

Contributor Information

Johnson Alfred Daniel, Department of Agricultural Science and Engineering, Otis L. Floyd Nursery Research Center, Tennessee State University, 472 Cadillac Lane, McMinnville, TN 37110, USA.

James B Woolley, Department of Entomology, Texas A&M University, 2475 TAMU, 370 Olsen Blvd, College Station, TX 77843-2475, USA.

Karla M Addesso, Department of Agricultural Science and Engineering, Otis L. Floyd Nursery Research Center, Tennessee State University, 472 Cadillac Lane, McMinnville, TN 37110, USA.

Author Contributions

J. Alfred Daniel (Conceptualization [equal], Data curation [equal], Formal analysis [equal], Methodology [equal], Writing—original draft [equal]), Karla Addesso (Conceptualization [equal], Funding acquisition [lead], Methodology [equal], Project administration [lead], Resources [lead], Supervision [lead], Writing—review & editing [lead]), and James Woolley (Investigation [equal], Resources [equal], Visualization [equal], Writing—review & editing [equal])

References

  1. Abd‐Rabou S. Revision of the genus Aphytis (Hymenoptera: Aphelinidae) with descriptions of two new species from Egypt. Insect Sci. 2004:11(2):149–164. 10.1111/j.1744-7917.2004.tb00189.x [DOI] [Google Scholar]
  2. Addesso KM, Blalock A, O’Neal PA.. Japanese maple scale activity and management in field nursery production. J Environ Hortic. 2016:34(2):41–46. 10.24266/0738-2898-34.2.41 [DOI] [Google Scholar]
  3. Addesso KM, O’Neal PA.. Evaluation of systemic pesticides as preventative treatments for Japanese maple scale, 2016-17. Arthropod Manag Tests. 2018:43(1):1–2. [Google Scholar]
  4. EPPO. Lopholeucaspis japonica. Global Database 2016; 2016. [accessed 2023 Aug 28]. https://gd.eppo.int/taxon/LOPLJA
  5. Flanders SE, Gressitt JL, Fisher TW.. Casca chinensis Howard, an internal parasite of the California red scale. Hilgardia. 1958:28(3):65–91. 10.3733/hilg.v28n03p065 [DOI] [Google Scholar]
  6. Frank SD, Klingeman WE, White SA, Fulcher A.. Biology, injury, and management of maple tree pests in nurseries and urban landscapes. J Integr Pest Manag. 2013:4(1):1–14. 10.1603/ipm12007 [DOI] [Google Scholar]
  7. Fulcher AFH, Halcomb M.. Japanese maple scale: An important new insect pest in the nursery and landscape. UT Extension Publication: W277; 2012. [accessed 2023 Oct 12]. https://trace.tennessee.edu/utk_agexgard/98/. [Google Scholar]
  8. García Morales M, Denno BD, Miller DR, Miller GL, Ben-Dov Y, Hardy NB.. ScaleNet: a literature-based model of scale insect biology and systematics; 2016: Database [accessed 2023 Oct 25]. 10.1093/database/bav118. http://scalenet.info. [DOI] [PMC free article] [PubMed]
  9. Gerson U. The natural enemies of the chaff scale, Parlatoria pergandii Comstock, in Israel. Entomophaga. 1967:12(2):97–109. 10.1007/bf02370606 [DOI] [Google Scholar]
  10. Gerson U. The comparative biologies of two hymenopterous parasites of the chaff scale, Parlatoria pergandeii. Entomophaga. 1968:13(2):163–173. 10.1007/bf02371787 [DOI] [Google Scholar]
  11. Gibson GAP, Huber JT, Woolley JB, editors. Annotated keys to the genera of Nearctic Chalcidoidea (Hymenoptera). Ottawa (Canada): National Research Council Research Press; 1997. [Google Scholar]
  12. Gilder K, Masloski KE, Woolley JB, Gu M, Michael E, Merchant ME, Heinz M.. Discovery of a non-native parasitoid, Marlattiella prima Howard (Hymenoptera, Aphelinidae) and its non-native host, Lopholeucaspis japonica Cockerell (Hemiptera, Diaspididae) in Central Texas. J Hymenopt Res. 2020:77:213–217. [Google Scholar]
  13. Gill S, Shrewsbury P, Davidson J.. Japanese maple scale: a pest of nursery and landscape trees and shrubs. UMD Extension Publication: FS-967-2014; 2014. [accessed 2023 Nov 1]. https://extension.umd.edu/resource/japanese-maple-scale-home-landscapes. [Google Scholar]
  14. Gordh G, Hall J.. A critical point drier used as a method of mounting insects from alcohol. Entomol News. 1979:90(1):57–59. [Google Scholar]
  15. Harsur MM, Joshi S, Pal RK.. Pomegranate: a new host for the invasive scale insect Lopholeucaspis japonica (Cockerell, 1897) (Hemiptera: Diaspididae) from Gujarat, India. Orient Insects. 2018:53(1):104–111. 10.1080/00305316.2018.1451783 [DOI] [Google Scholar]
  16. Hunter MS, Woolley JB.. Evolution and behavioral ecology of heteronomous aphelinid parasitoids. Annu Rev Entomol. 2001:46:251–290. 10.1146/annurev.ento.46.1.251 [DOI] [PubMed] [Google Scholar]
  17. Japoshvili G, Abell KJ, Normark BB, Driesche RGV.. Aphelinid and encyrtid (Hymenoptera: Chalcidoidea) parasitoids of armored scales (Hemiptera: Diaspididae) attacking hemlocks (Tsuga spp.) in Japan and the United States, with description of eight new species. Ann Entomol Soc Am. 2013:106(5):541–554. 10.1603/an13023 [DOI] [Google Scholar]
  18. Jeger M, Bragard C, Caffier D, Candresse T, Chatzivassiliou E, Dehen-Schnutz K, Gilioli G, Grégore J, Jaques Miret JA, Navarro MN, et al. Pest categorization of Lopholeucaspis japonica. EFSA J. 2018:16(7):e05353. 10.2903/j.efsa.2018.5353 [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kim JW, Heraty J.. A phylogenetic analysis of the genera of Aphelininae (Hymenoptera: Aphelinidae), with a generic key and descriptions of new taxa. Syst Entomol. 2012:37(3):497–549. 10.1111/j.1365-3113.2012.00625.x [DOI] [Google Scholar]
  20. Krombein KV, Hard PD, Smith DR, Burks BD.. Catalog of hymenoptera in America north of Mexico, Vol. 1. Washington DC: Smithsonian Institution Press; 1979. [Google Scholar]
  21. Miller DR, Davidson JA.. Armored scale insect pests of trees and shrubs. Ithaca (New York): Cornell University Press; 2005. [Google Scholar]
  22. Miller DR, Miller GL, Hodges GS, Davidson JA.. Introduced scale insects (Hemiptera: Coccoidea) of the United States and their impact on U.S. agriculture. Proc Entomol Soc Wash. 2005:107(1):123–158. [Google Scholar]
  23. Noyes JS. Collecting and preserving chalcid wasps (Hymenoptera: Chalcidoidea). J Nat Hist. 1982:16(3):315–334. 10.1080/00222938200770261 [DOI] [Google Scholar]
  24. Rosen D, DeBach P.. Notes on the genus Marlattiella Howard (Hymenoptera: Aphelinidae). Mushi. 1970:43(3):39–43. [Google Scholar]
  25. Rosen D, DeBach P.. Species of Aphytis of the world: Hymenoptera: Aphelinidae Series Entomologica, Vol. 17. Berlin (Germany): Springer Dordrecht; 1979. [Google Scholar]
  26. Shrewsbury PM, Harding NM, Rojas MS, Gill S.. Japanese maple scale: woody ornamental host plants. UMD Extension Publication: EBR-01-2020; 2020. [accessed 2023 Nov 1]. https://extension.umd.edu/resource/japanese-maple-scale-woody-ornamental-host-plants. [Google Scholar]
  27. Suh S-J, Evans GA.. Revision of the list of aphelinids (Hymenoptera: Aphelinidae) in South Korea and analysis of their relevance as biological control agents for the EPPO region. EPPO Bull. 2019:49(2):380–385. 10.1111/epp.12566 [DOI] [Google Scholar]
  28. Tachikawa T. Discovery of Marlatiella prima Howard, a parasite of the pear scale from Japan (Hymenoptera: Aphelinidae). Trans Shikoku Entomol Soc. 1962a:7(3):74–77. [Google Scholar]
  29. Universal Chalcidoidea Database Curators. Universal Chalcidoidea Database Web (UCDW) curated in TaxonWorks; 2023. [accessed 2023 Oct 29]. https://www.nhm.ac.uk/our-science/data/chalcidoids/database/.
  30. Woolley JB, Browning HW.. Morphometric analysis of uniparental Aphytis reared from chaff scale, Parlatoria pergandei Comstock, on Texas citrus (Hymenoptera: Aphelinidae, Homoptera: Diaspididae). Proc Entomol Soc Wash. 1987:89(1):77–94. [Google Scholar]
  31. Xu ZH, Huang J.. Chinese fauna of parasitic wasps on scale insects. China: National Natural Science Foundation of China; 2004. [Google Scholar]
  32. Yasnosh VA. The biosystematic characteristics of species of the genus Aphytis Howard (Chalcidoidea, Aphelinidae), parasites of scale-insects in the USSR. Entomol Obozr. 1972:51(2):240–253. [Google Scholar]
  33. Yasnosh VA. Hymenoptera II. Chalcidoidea 15. Aphelinidae. Opredeliteli Nasekomykh Evropeyskoy Chasti SSR, Vol. 3. Moscow: Nuaka; 1978. p. 469–501. [Google Scholar]
  34. Zang LS, Liu TX, Wan FH.. Reevaluation of the value of autoparasitoids in biological control. PLoS One. 2011:6(5):e20324. 10.1371/journal.pone.0020324 [DOI] [PMC free article] [PubMed] [Google Scholar]

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