Print
Updated list of the insect parasitoids (Insecta, Hymenoptera) associated with Lobesia botrana (Denis & Schiffermüller, 1775) (Lepidoptera, Tortricidae) in Italy. 2. Hymenoptera, Ichneumonidae, Anomaloninae and Campopleginae
expand article infoPier Luigi Scaramozzino, Filippo Di Giovanni, Augusto Loni, Renato Ricciardi, Andrea Lucchi
‡ University of Pisa, Pisa, Italy
Open Access

Abstract

In this second review of the parasitoids recorded on Lobesia botrana (EGVM) in Italy, an updated list and summary of the information available on 14 taxa of Ichneumonidae belonging to the subfamilies Anomaloninae and Campopleginae are provided. For each taxon, geographic distributions, host ranges, ecological role in viticulture and/or in other crops, and taxonomy are provided and discussed. For the most interesting species, tables summarizing the parasitization rates recorded in the field on EGVM or other lepidopteran pests are given. Identification mistakes and wrong synonymies that have generated great confusion and often made geographic distributions and host ranges unreliable are highlighted. A list of four Anomaloninae and 27 Campopleginae recorded on EGVM in Europe is also provided. Among the species examined, Campoplex capitator Aubert is the only potential candidate for biological control of EGVM.

Keywords

Biological control, Campoplex capitator, European grapevine moth, ichneumonid wasps, natural enemies, taxonomy

Introduction

A general overview of the parasitoids of Lobesia botrana (Denis & Schiffermüller, 1775) (European grapevine moth, EGVM) recorded in Italy, including Diptera Tachinidae and Hymenoptera Braconidae, has been recently published (Scaramozzino et al. 2017a). This second contribution deals with two subfamilies of Ichneumonidae, the Anomaloninae and Campopleginae.

Materials and methods

As in the previous contribution (Scaramozzino et al. 2017a), the list of Ichneumonidae living on EGVM in Italy has been compiled using all the documents published on the subject, both in Italy (Table 1) and worldwide. As previously done, we also reviewed the parasitoid lists compiled by Thompson (1946), Coscollá (1997), Hoffmann and Michl (2003), and CABI (2017). The names of the species have been checked and updated according to the following databases: Taxapad (Yu et al. 2012), Noyes (2017) and Fauna Europaea (de Jong et al. 2014). In addition, material from the following private collections has been examined: J-F. Aubert at the Musée Cantonal de Zoologie in Lausanne (Switzerland), K. Horstmann at the Zoologische Staatssammlung in Munich (Germany, ZSM), F. Silvestri at the Department of Agriculture in Portici (Naples, Italy).

Bibliography consulted for the compilation of the parasitoid list of EGVM in Italy. See paper references for the full bibliographic citation. The numbers on the left are the same as in Table 2.

1 Bagnoli B, Lucchi A (2006)
2 Boselli F (1928)
3 Catoni G (1910)
4 Catoni G (1914)
5 Catoni G (1915)
6 Colombera S, Alma A, Arzone A (2001)
7 Dalla Montà L, Marchesini E, Bagnoli B, Goggioli D (1993)
8 Del Guercio G (1899)
9 Delrio G, Luciano P, Prota R (1987)
10 Forti D (1991)
11 Leonardi G (1925)
12 Loni A, Samartsev KG, Scaramozzino PL, Belokobylskij SA, Lucchi A (2016)
13 Lozzia GC, Rigamonti IE (1991)
14 Lucchi A, Santini L (2011)
15 Luciano P, Delrio G, Prota R (1988)
16 Marchesini E (2007)
17 Marchesini E, Dalla Montà L (1992)
18 Marchesini E, Dalla Montà L (1994)
19 Marchesini E, Dalla Montà L (1998)
20 Marchesini E, Dalla Montà L, Sancassani GP (2006)
21 Nuzzaci G, Triggiani O (1982)
22 Pinna M, Gremo F, Scaramozzino PL (1989)
23 Roat C, Forti D (1994)
24 Ruschka F, Fulmek L (1915)
25 Scaramozzino PL, Loni A, Lucchi A, Gandini L (2017b)
26 Schwangart F (1913)
27 Schwangart F (1918)
28 Silvestri F (1912)
29 Stellwaag F (1921)
30 Stellwaag F (1928)
31 Zangheri S, Dalla Montà L, Duso C (1987)

Results

From late 1800s to date, 120 ichneumonid species belonging to 51 distinct genera and ten subfamilies were reported on EGVM (Stellwaag 1928, Thompson 1946, Hoffmann and Michl 2003, Yu et al. 2012). In 1946, Thompson listed 60 ichneumonids associated to EGVM; since then, the number of species has almost doubled. Taxapad (Yu et al. 2012) reports 69 species, whereas Hoffmann and Michl (2003) provide the most complete list, with 94 species recorded. In our comprehensive list of 63 taxa reported for Italy (Table 2), the subfamily with the greatest number of taxa is Cryptinae (20), followed by Campopleginae (11), Pimplinae (10), Ichneumoninae (9), Metopiinae (7), Anomaloninae (3), Tryphoninae (2) and Cremastinae (1).

List of Ichneumonidae (Hymenoptera) parasitoids of EGVM reported in Italy. Valid names are in bold. Synonyms, misspellings, combinations other than those valid today are preceded by a dot. Numbers are referred to Authors shown in Table 1. In two separate columns we indicated if the record is earlier or later than 1970. NORTH includes Aosta Valley, Piedmont, Liguria, Lombardy, Trentino-South Tyrol, Veneto, Friuli-Venezia Giulia and Emilia-Romagna regions; CENTER includes Tuscany, Marche, Umbria, Lazio and Abruzzo regions; SOUTH includes Campania, Molise, Apulia, Basilicata and Calabria regions.

Species Subfamily <1970 >1970 NORTH CENTER SOUTH SICILY SARDINIA
Agrothereutes sp. Cryptinae [13] (Spilocryptus sp.), [22] [13] (Spilocryptus sp.), [22]
Agrothereutes abbreviator (Fabricius, 1798) = emendation for Agrothereutes abbreviatus (Fabricius, 1794)
Agrothereutes abbreviatus (Fabricius, 1794) Cryptinae [16, 17, 19, 20, 23] (A. abbreviator) [16, 18, 19, 20, 23] (A. abbreviator)
Agrothereutes pumilus (Kriechbaumer, 1899) Cryptinae [6, 9] [6] [9]
Agrypon flaveolatum (Gravenhorst, 1807) Anomaloninae [26, 29, 30] [26, 29, 30]
Angitia tenuipes Thomson, 1887 = syn. Diadegma tenuipes (Thomson, 1887)
Angitia tibialis (Gravenhorst, 1829) = syn. Diadegma armillatum (Gravenhorst, 1829)
Aptesis nigrocincta (Gravenhorst, 1815) Cryptinae [30] (Helcostizus nigrocinctus), [2, 26, 29] (Microcryptus nigrocinctus), [11] (Microcryptus nigrolineatus), [3, 4, 5, 28] (Microcryptus nigrotinctus) [30] (Helcostizus nigrocinctus), [26, 29] (Microcryptus nigrocinctus), [3, 4, 5] (Microcryptus nigrotinctus)
Atrometus geniculatus (Holmgren, 1857) = syn. Parania geniculata (Holmgren, 1857)
Bathythrix argentata (Gravenhorst, 1829) Cryptinae [9, 16, 19, 20] [16, 19, 20] [9]
Bathythrix decipiens (Gravenhorst, 1829) Cryptinae [16, 17, 18, 19, 20, 32] [16, 17, 18, 19, 20, 32]
Cambrus inferus = misspelling for Gambrus inferus Thomson, 1896
Campoplex sp. Campopleginae [13, 22] [13, 22]
Campoplex borealis (Zetterstedt, 1838) Campopleginae [21] [21]
* Campoplex capitator Aubert, 1960 Campopleginae [3, 4, 5, 11, 28, 30] (Omorgus difformis), [2] (Omurgus difformis) [1, 6, 7, 12, 14, 16, 17, 18, 19, 20, 25] [6, 7, 16, 17, 18, 19, 20], [3, 4, 5, 28] (Omorgus difformis) [1, 12, 14, 25] [28, 30] (Omorgus difformis)
* Campoplex difformis (Gmelin, 1790) Campopleginae [24, 26, 29, 30] (Omorgus difformis) [21] [24, 26, 29, 30] (Omorgus difformis) [21]
Cinxaelotus erythrogaster Holmgren, 1890 =syn. Dicaelotus erythrogaster (Holmgren, 1890)
Cryptus sp. Cryptinae [13] [13]
Diadegma armillatum (Gravenhorst, 1829) Campopleginae [28, 30] (Angitia tibialis) [28, 30] (Angitia tibialis)
Diadegma tenuipes (Thomson, 1887) Campopleginae [2, 3, 4, 5, 11, 26, 28, 30, 31] (Angitia tenuipes) [3, 4, 5, 26, 30, 31] (Angitia tenuipes)
Diadromus collaris (Gravenhorst, 1829) Ichneumoninae [30] (Thyraeella collaris), [28] (Thyrella collaris) [30] (Thyraeella collaris), [28] (Thyrella collaris)
Dicaelotus sp. Ichneumoninae [13, 22, 23] [13, 22, 23]
Dicaelotus erythrogaster (Holmgren, 1890) Ichneumoninae [2, 3, 4, 5, 11, 24, 26, 28, 29, 30, 31] (Cinxaelotus erythrogaster) [3, 4, 5, 24, 26, 29, 30, 31] (Cinxaelotus erythrogaster)
Dicaelotus inflexus Thomson, 1891 Ichneumoninae [2, 4, 5, 7, 28, 30, 31] (D. resplendens) [1, 6, 16, 17, 18, 19, 20], [9, 32] (D. resplendens) [6, 7, 16, 17, 18, 19, 20], [4, 5, 28, 30, 31, 32] (D. resplendens) [1] [28, 30] (D. resplendens) [9] (D. resplendens)
Dicaelotus pusillator (Gravenhorst, 1807) Ichneumoninae [8, 11, 28, 29, 30] [29, 30]
Dicaelotus resplendens Holmgren, 1890 = misidentification for Dicaelotus inflexus Thomson, 1891 (see Marchesini and Dalla Montà 1994)
Endromopoda detrita (Holmgren, 1860) Pimplinae [2, 3, 4, 5, 11, 26, 28, 29, 30, 31] (Pimpla detrita) [3, 4, 5, 26, 28, 29, 30, 31] (Pimpla detrita)
Exochus sp. Metopiinae [1] [1]
Exochus lentipes Gravenhorst, 1829 Metopiinae [29] (E. notatus) [25] (E. notatus) [29] (E. notatus) [25] (E. notatus)
Exochus notatus Holmgren, 1858 = syn. Exochus lentipes Gravenhorst, 1829
Exochus tibialis Holmgren, 1858 Metopiinae [2, 4, 5, 26, 29, 30, 31] [13, 16, 18, 19, 20, 22] [4, 5, 13, 16, 18, 19, 20, 22, 26, 29, 30, 31]
Eulimneria alkae (Ellinger & Sachtleben, 1928) = syn. Sinophorus turionum (Ratzeburg, 1844)
Eulimneria crassifemur (Thomson, 1887) = syn. Sinophorus crassifemur (Thomson, 1887)
Eulimneria ramifemur = misspelling for Sinophorus crassifemur (Thomson, 1887)
Gambrus infernus = misspelling for Gambrus inferus Thomson, 1896
Gambrus inferus Thomson, 1896 = syn. Gambrus ornatus (Gravenhorst, 1829)
Gambrus ornatus (Gravenhorst, 1829) Cryptinae [26] (Cambrus inferus), [29] (G. infernus), [2, 3, 4, 5, 11, 28, 30, 31] (G. inferus) [26] (Cambrus inferus), [29] (G. infernus), [3, 4, 5, 30, 31] (G. inferus)
Gelis sp. Cryptinae [22] [22]
Gelis acarorum (Linnaeus, 1758) Cryptinae [31] (Gelis sericeus), [3, 4, 5, 24, 26, 28, 30] (Pezomachus sericeus) [31] (Gelis sericeus), [3, 4, 5, 24, 26, 30] (Pezomachus sericeus)
Gelis areator (Panzer, 1804) Cryptinae [3, 4, 5, 11, 26, 28, 29, 30] (Hemiteles areator), [29, 30] (Hemiteles pulchellus) [6, 16, 18, 19, 20] [3, 4, 5, 26, 29, 30] (Hemiteles areator), [29, 30] (Hemiteles pulchellus), [6, 16, 18, 19, 20]
Gelis cinctus (Linnaeus, 1758) Cryptinae [16, 17, 18, 19, 20, 32] [16, 17, 18, 19, 20, 32]
Gelis sericeus (Förster, 1850) = syn. Gelis acarorum (Linnaeus, 1758)
Habrocryptus alternator (Gravenhorst, 1829) = syn. Ischnus alternator (Gravenhorst, 1829)
Habrocryptus punctiger Thomson, 1896 = syn. Ischnus migrator (Fabricius, 1775)
Habrocyptus punctiger = misspelling for Habrocryptus punctiger Thomson, 1896
Habrocryptus puntiger = misspelling for Habrocryptus punctiger Thomson, 1896
Helcostizus nigrocinctus (Gravenhorst, 1815) = syn. Aptesis nigrocincta (Gravenhorst, 1815)
Hemiteles sp. Cryptinae [8, 13] [9] [13] [9]
Hemiteles areator (Panzer, 1804) =syn. Gelis areator (Panzer, 1804)
Hemiteles hemipterum (Fabricius, 1793) = misspelling for Hemiteles hemipterus (Fabricius, 1793)
Hemiteles hemipterus (Fabricius, 1793) = syn. Theroscopus hemipteron (Riche, 1791)
Hemiteles nigriventris Thomson, 1884 = syn. Isadelphus gallicola (Bridgman, 1880)
Hemiteles pulchellus Gravenhorst, 1829 = syn. Gelis areator (Panzer, 1804)
Hemiteles sordipes Gravenhorst, 1829 = syn. Mastrus sordipes (Gravenhorst, 1829)
Herpestomus furunculus Wesmael, 1845 = syn. Herpestomus nasutus Wesmael, 1845
Herpestomus sp. Ichneumoninae [24, 30] [24, 30]
Herpestomus nasutus Wesmael, 1845 Ichneumoninae [2, 3, 4, 5, 11, 26, 28, 29, 30] (H. furunculus) [3, 4, 5, 26, 29, 30] (H. furunculus)
Isadelphus sp. Cryptinae [23] [23]
Isadelphus gallicola (Bridgman, 1880) Cryptinae [26, 29, 30] (Hemiteles nigriventris) [26, 29, 30] (Hemiteles nigriventris)
Ischnus sp. Cryptinae [6] [6]
Ischnus alternator (Gravenhorst, 1829) Cryptinae [2, 4, 5, 26, 29, 30, 31] (Habrocryptus alternator) [1, 13, 16, 17, 18, 19, 20, 22, 32] [4, 5, 26, 29, 30, 31] (Habrocryptus alternator), [13, 16, 17, 18, 19, 20, 22, 32] [1]
Ischnus migrator (Fabricius, 1775) Cryptinae [2, 3, 31] (Habrocytus punctiger), [2, 11, 26, 29, 30, 31] (Habrocryptus punctiger), [4, 5] (Habrocryptus puntiger) [3, 31] (Habrocytus punctiger), [26, 29, 30, 31] (Habrocryptus punctiger), [4, 5] (Habrocryptus puntiger)
Itoplectis sp. Pimplinae [11] [11]
Itoplectis alternans (Gravenhorst, 1829) Pimplinae [2, 3, 4, 5, 11, 24, 26, 28, 29, 30, 31] (Pimpla alternans) [6, 9, 16, 17, 18, 19, 20, 22, 23, 25] [3, 4, 5, 24, 26, 28, 29, 30, 31] (Pimpla alternans), [6, 16, 17, 18, 19, 20, 22, 23] [25] [28, 30] (Pimpla alternans) [9]
Itoplectis maculator (Fabricius, 1775) Pimplinae [2, 4, 5, 26, 29, 30] (Pimpla maculator) [1] [4, 5, 26, 29, 30] (Pimpla maculator) [1]
Itoplectis tunetana (Schmiedeknecht, 1914) Pimplinae [16, 17, 18, 19, 20, 22, 25, 32] [16, 17, 18, 19, 20, 22, 32] [25]
Linycus exhortator (Fabricius, 1787) Ichneumoninae [26, 29, 30] (Platylabus dimidiatus) [26, 29, 30] (Platylabus dimidiatus)
Mastrus sordipes (Gravenhorst, 1829) Cryptinae [2, 4, 5, 26, 29, 30] (Hemiteles sordipes) [4, 5, 26, 29, 30] (Hemiteles sordipes)
Microcryptus nigrocinctus (Gravenhorst, 1815) = syn. Aptesis nigrocincta (Gravenhorst, 1815)
Microcryptus nigrolineatus = misspelling for Microcryptus nigrocinctus (Gravenhorst, 1815)
Microcryptus nigrotinctus = misspelling for Microcryptus nigrocinctus (Gravenhorst, 1815)
Nemeritis sp. Campopleginae [8]
Omorgus difformis (Gmelin, 1790) = syn. Campoplex difformis (Gmelin, 1790)
Omurgus difformis = misspelling for Omorgus difformis (Gmelin, 1790)
Parania geniculata (Holmgren, 1857) Anomaloninae [28, 30] (Atrometus geniculatus) [28, 30] (Atrometus geniculatus)
Pezomachus sericeus Förster, 1850 = syn. Gelis acarorum (Linnaeus, 1758)
Phaeogenes sp. Ichneumoninae [2, 4, 5, 26, 29, 30] [4, 5, 26, 29, 30]
Phytodiaetus sp. = misspelling for Phytodietus sp.
Phytodietus sp. Tryphoninae [1, 16, 18, 19, 20] (Phytodiaetus sp.) [16, 18, 19, 20] (Phytodiaetus sp.) [1] (Phytodiaetus sp.)
Phytodietus pleuralis Cresson, 1865 = North-American species, errouneously reported for Italy in Leonardi (1925), after Silvestri (1912)
Phytodietus polyzonias (Förster, 1771) Tryphoninae [6], [15] (Phytodietus segmentator) [6] [15] (Phytodietus segmentator)
Phytodietus segmentator Gravenhorst, 1829 = syn. Phytodietus polyzonias (Förster, 1771)
Pimpla sp. Pimplinae [13] [13]
Pimpla alternans Gravenhorst, 1829 = syn. Itoplectis alternans (Gravenhorst, 1829)
Pimpla apricaria Costa, 1885 Pimplinae [9] [9]
Pimpla detrita Holmgren, 1860 = syn. Endromopoda detrita (Holmgren, 1860)
Pimpla examinator (Fabricius, 1804) = syn. Pimpla turionellae (Linnaeus, 1758)
Pimpla maculator (Fabricius, 1775) = syn. Itoplectis maculator (Fabricius, 1775)
Pimpla spuria Gravenhorst, 1829 Pimplinae [2, 3, 4, 5, 11, 26, 28, 29, 30, 31] (P. strigipleuris) [1, 6, 16, 17, 18, 19, 20, 22, 23] [6, 16, 17, 18, 19, 20, 22, 23], [3, 4, 5, 26, 29, 30, 31] (P. strigipleuris) [1]
Pimpla strigipleuris Thomson, 1877 = syn. Pimpla spuria Gravenhorst, 1829
Pimpla turionellae (Linnaeus, 1758) Pimplinae [2, 4, 5, 8, 11, 26, 28, 29, 30, 31], [2, 4, 5, 26, 28, 29, 30] (P. examinator) [9, 16, 18, 19, 20, 32] [4, 5, 16, 18, 19, 20, 26, 28, 29, 30, 31, 32], [4, 5, 26, 28, 29, 30] (P. examinator) [28, 30] [9]
Platylabus dimidiatus (Gravenhorst, 1829) = syn. Lynicus exhortator (Fabricius, 1787)
Pristomerus vulnerator (Panzer, 1799) Cremastinae [9, 16, 18, 19, 20] [16, 18, 19, 20] [9]
Scambus elegans (Woldstedt, 1877) Pimplinae [9] [9]
Sinophorus crassifemur (Thomson, 1887) Campopleginae [29, 30] (Eulimneria crassifemur) [26, 29] (Eulimneria ramifemur) [29, 30] (Eulimneria crassifemur) [26, 29] (Eulimneria ramifemur)
Sinophorus turionum (Ratzeburg, 1844) Campopleginae [31] (Eulimneria alkae)
Spilocryptus sp. = syn. Agrothereutes sp.
Theroscopus hemipteron (Riche, 1791) Cryptinae [26] (Hemiteles hemipterum), [2, 4, 5, 29, 30] (Hemiteles hemipterus) [1, 9, 16, 18, 19, 20, 32] (T. hemipterus) [26] (Hemiteles hemipterum), [4, 5, 29, 30] (Hemiteles hemipterus), [16, 18, 19, 20, 32] (T. hemipterus) [1] (T. hemipterus) [9] (T. hemipterus)
Theroscopus hemipterus (Fabricius, 1793) = syn. Theroscopus hemipteron (Riche, 1791)
Thyraeella collaris (Gravenhorst, 1829) = syn. Diadromus collaris (Gravenhorst, 1829)
Thyrella collaris = misspelling for Thyraeella collaris (Gravenhorst, 1829)
Tranosemella praerogator (Linnaeus, 1758) Campopleginae [6, 7, 16, 18, 19, 20] [6, 7, 16, 18, 19, 20]
Trichomma enecator (Rossi, 1790) Anomaloninae [6, 25] [6] [25]
Triclistus sp. Metopiinae [1, 15, 17, 23] [17, 23] [1] [15]
Triclistus albicinctus Thomson, 1887 Metopiinae [16, 18, 19, 20] [16, 18, 19, 20]
Triclistus lativentris Thomson, 1887 Metopiinae [9] [9]
Triclistus nitidifrons = misspelling for Triclistus nitifrons Thomson, 1887
Triclistus nitifrons Thomson, 1887 = syn. Triclistus pallipes Holmgren, 1873
Triclistus pallidipes = misspelling for Triclistus pallipes Holmgren, 1873
Triclistus pallipes Holmgren, 1873 Metopiinae [28] (T. nidifrons), [8, 11] (T. nitidifrons), [28, 30] (T. pallidipes) [25] [25] [28, 30] (T. pallidipes)
Venturia canescens (Gravenhorst, 1829) Campopleginae [16, 18, 19, 20] [16, 18, 19, 20]

In the present work, we focus on the ichneumonid subfamilies Anomaloninae and Campopleginae. So far, four taxa of Anomaloninae and 27 of Campopleginae have been associated with EGVM (Table 3).

Ichneumonidae Anomaloninae and Campopleginae reported by various authors as living at the expense of the European grapevine moth.

Valid names Name reported by the author/s Author/s and year of publication Country
ANOMALONINAE
1 Agrypon anxium (Wesmael,1849) Agrypon anxium (Wesmael,1849) Moreau et al. 2010 France, Switzerland
2 Agrypon flaveolatum (Gravenhorst, 1807) Agrypon flaveolatum Schwangart 1913, 1918 Germany (Palatinate), Italy (South Tyrol)
Agrypon (Anomalon) flaveolatum Feytaud 1913 Germany
Agrypon flaveolatum Grav. Stellwaag 1921 Germany (Franconia and Rhineland- Palatinate), Italy (South Tyrol)
Agrypon flaveolatum Grav. Stellwaag 1928
Agrypon flaveolatum Grav. Thompson 1946 Austria, France, Germany
3 Parania geniculata (Holmgren, 1857) Atrometus geniculatus Forst. Silvestri 1912 Italy (South Tyrol)
Atrometus geniculatus Först. Stellwaag 1928 Italy (South Tyrol)
Sinophorus geniculatus Grav. Hoffmann and Michl 2003
4 Trichomma enecator (Rossi, 1790) Trichomma enecator (Rossi 1790) Telenga 1934 Crimea
Trichomma enecator (Rossi 1790) Colombera et al. 2001 Italy (Piedmont)
Trichomma enecator Scaramozzino et al. 2017b Italy (Tuscany)
CAMPOPLEGINAE
1 Campoplex abbreviatus (Brischke, 1880) Mesoleius (Omorgus) abbreviatus Brischke Stellwaag 1928 (after Schwangart)
Campoplex abbreviatus Brischke Thompson 1946 France
Campoplex abbreviatus Brisch. Hoffmann and Michl 2003
2 Campoplex borealis (Zetterstedt, 1838) Campoplex borealis CABI 2017
3 Campoplex capitator Aubert, 1960 Campoplex capitator CABI 2017
Campoplex capitator Aubert Hoffmann and Michl 2003
Campoplex capitator Aub. Koclu et al. 2005 Turkey
Campoplex capitator Aubert,1960 Villemant et al. 2011 France, Italy, Portugal, Spain
Campoplex capitator Aubert,1960 Yu et al. 2012
4 Campoplex difformis (Gmelin, 1790) Omorgus difformis (Gmel.) Thoms Stellwaag 1928 (after Rübsaamen, Marchal, Catoni, Schwangart, Feytaud, Silvestri, Ruschka and Fulmek, Dobredev, Voukassovitch) Italy (South Tyrol),Austria
Omorgus difformis Gm. Telenga 1934 Crimea
Campoplex difformis Grav. Thompson 1946 (after Telenga) Austria, France, Germany, Italy, Crimea
4 Campoplex difformis (Gmelin, 1790) Campoplex difformis Gmelin Hoffmann and Michl 2003
Campoplex difformis CABI 2017
Campoplex difformis (Gmelin,1790) Yu et al. 2012
5 Campoplex sp. Campoplex sp. Thompson 1946 France
6 Diadegma areolare (Holmgren, 1860) Angitia areolaris (Holmgr.) Thoms. Stellwaag 1928 (after Rübsaamen, Schwangart, Dobredev)
Angitia areolaris Hlgr. Thompson 1946 Russia
7 Diadegma armillatum (Gravenhorst, 1829) Angitia (Dioctes) tibialis Grav. Stellwaag 1928 (after Silvestri) Italy
Diadegma armillatum Grav. Hoffmann and Michl 2003
8 Diadegma fenestrale (Holmgren, 1860) Angitia fenestralis (Holmgr.) Thoms. Stellwaag 1928(after Rübsaamen,Schwangart,Dobredev)
Angitia fenestralis Hlgr. Thompson 1946 Russia
Diadegma fenestrale Holm. Hoffmann and Michl 2003
Diadegma fenestrale (Holmgren,1860) Villemant et al. 2011 France, Germany, Switzerland
9 Diadegma majale (Gravenhorst,1829) Marchal 1912, Feytaud 1913 France
10 Diadegma melanium (Thomson, 1887) Angitia melania Thoms. Stellwaag 1928 (after Marchal) France (envir. Paris)
Angitia melania Thoms. Thompson 1946 Russia
Diadegma melanium Thoms. Hoffmann and Michl 2003
11 Diadegma holopygum (Thomson, 1887) Diadegma holopygum (Thomson 1887) Yu et al. 2012
Diadegma holopyga (Thoms.) Bărbuceanu and Jenser 2009 Romania (South)
12 Diadegma longicaudatum Horstmann, 1969 Diadegma longicaudatum Horstmann 1969 Yu et al. 2012
Diadegma longicaudata Horst. Bărbuceanu and Jenser 2009 Romania (South)
13 Diadegma sp. Angitia sp. Thompson 1946 France
14 Diadegma tenuipes (Thomson, 1887) Angitia tenuipes Thoms. Stellwaag 1928 (after Catoni, Schwangart) Italy (South Tyrol)
Angitia tenuipes Thoms. Thompson 1946 Italy
Diadegma tenuipes Thoms. Hoffmann and Michl 2003
Diadegma tenuipes (Thomson 1887) Yu et al. 2012
Diadegma tenuipes (Thoms.) Bărbuceanu and Jenser 2009 Romania (South)
15 Diadegma trochanteratum (Thomson, 1887) Angitia trochanterata Thoms. Stellwaag 1928(after Schwangart)
Diadegma trochanteratum Thoms. Hoffmann and Michl 2003
16 Enytus apostata (Gravenhorst, 1829). Angitia exareolata (Ratzebg.) Thoms. Stellwaag 1928 (after Rübsaamen, Marchal, Dobredev)
Diadegma exareolatus Feytaud 1913 (after Marchal) France
Angitia exareolata Ratz. Thompson 1946 Russia
16 Enytus apostata (Gravenhorst, 1829). Enytus apostatus Grav. Hoffmann and Michl 2003
Enytus apostatus (Gravenhorst 1829) Yu et al. 2012
Enytus apostata Gravenhorst Lotfalizadeh et al. 2012 Iran
Diadegma apostata (Grav.) Bărbuceanu and Jenser 2009 Romania (South)
17 Enytus obliteratus (Cresson, 1864) Enytus obliteratus (Cresson 1864) Yu et al. 2012
18 Hyposoter ebeninus (Gravenhorst, 1829) Anilastus ebeninus Grav. Telenga 1934 Crimea
Anilastus ebeninus Grav. Thompson 1946 Russia
Hyposoter ebeninus (Gravenhorst 1829) Yu et al. 2012
19 Lathrostizus lugens (Gravenhorst, 1829) Angitia vestigialis (Ratzbg.) Thoms Stellwaag 1928 (after Rübsaamen, Marchal, Feytaud, Dobredev)
Angitia vestigialis, Ratz. Marchal 1912 France
Diadegma vestigialis Feytaud 1913 (after Marchal) France
Angitia vestigialis Ratz. Thompson 1946 Russia
Lathrostizus lugens Grav. Hoffmann and Michl 2003
20 Meloboris collector (Thunberg, 1822) Nepiera collector Thnbg. Thompson 1946 France
Nepiera concinna Hlgr. Faure 1925 France
Meloboris collector Thunberg Hoffmann and Michl 2003
Meloboris collector (Thunberg 1822) Yu et al. 2012
[Olesicampe argentata (Gravenhorst, 1829)] Olesicampe argentata Grav. Hoffmann and Michl 2003 Wrong record based on incorrect synonymy
21 Olesicampe sp. Limneria spec. Feytaud 1913 France
Olesicampe Förster Hoffmann and Michl 2003
22 Sinophorus costalis (Thomson, 1887) Sinophorus costalis Thoms. Pisicá and Páişescu-Bărbuceanu 2002 Romania
23 Sinophorus crassifemur (Thomson, 1887) Sinophorus crassifemur (Thomson 1887) Yu et al. 2012
[Sinophorus geniculatus (Gravenhorst, 1829)] Sinophorus geniculatus Grav. Hoffmann and Michl 2003 Wrong record based on incorrect synonymy
24 Sinophorus turionum (Ratzeburg, 1844) Eulimneria alkae E. and S. Thompson 1946 Austria, France, Germany, Italy
Sinophorus turionum Ratzeburg Hoffmann and Michl 2003
Campoplex alkae CABI 2017
Sinophorus turionum (Ratzeburg 1844) Yu et al. 2012
25 Tranosemella praerogator (Linnaeus, 1758) Tranosemella praerogator CABI 2017
Tranosemella praerogator Linn. Hoffmann and Michl 2003
Tranosemella praerogator (Linnaeus 1758) Villemant et al. 2011 France, Italy
Tranosemella praerogator (Linnaeus 1758) Yu et al. 2012
26 Venturia canescens (Gravenhorst, 1829) Venturia canescens Grav. Hoffmann and Michl 2003
Venturia canescens (Gravenhorst 1829) Thiéry et al. 2001, Villemant et al. 2011 France, Italy
Venturia canescens (Gravenhorst 1829) Yu et al. 2012
27 Venturia sp. Venturia sp. Koclu et al. 2005 Turkey

Order: HYMENOPTERA

Superfamily: ICHNEUMONOIDEA

Family: ICHNEUMONIDAE

Subfamily: Anomaloninae

Agrypon flaveolatum (Gravenhorst, 1807)

Agrypon flaveolatum: Schwangart 1913: 6, 1918: 547.

Agrypon flaveolatum: Stellwaag 1921: 85-86.

Italian distribution of reared parasitoids

Trentino-South Tyrol: Schwangart 1913, 1918; Stellwaag 1921.

Distribution

Species of temperate-cold zones of the Palearctic region, widespread in Europe (excluding the Balkan Peninsula), Russia, Turkey, eastwards to Korea and Japan (Yu et al. 2012). From Europe it has been introduced in Canada from 1956 to 1958 and from 1979 to 1981 to control the winter moth Opheroptera brumata (Linnaeus, 1758) (Lepidoptera, Geometridae) and has been reported as being established there (Carlson 1979, Barron 1989).

Host range

Yu et al. (2012) list 58 species, mostly belonging to the Lepidopteran family Geometridae (27 species). Further records include Tortricidae (8 species), Yponomeutidae (7), Noctuidae (5), Lasiocampidae, Nolidae (2 species each), Pyralidae, Thyatiridae, Notodontidae, Lycaenidae, Erebidae (Lymantria dispar (Linnaeus, 1758)), and Diprionidae (Hymenoptera Symphyta) (1 species each).

Ecological role

This larval-pupal koinobiont endoparasitoid emerged from overwintering pupae of L. botrana and Eupoecilia ambiguella (Hübner, 1796) (Stellwaag 1928, Thompson 1957) in Italy (South Tyrol), France and Germany and Sparganothis pilleriana (Denis & Schiffermüller, 1775) (Lepidoptera Tortricidae) in France (Stellwaag 1928). These hosts are not included in the list of Yu et al. (2012). Another species of the same genus, Agrypon anxium (Wesmael, 1849), is reported on the first generation larvae of EGVM in Switzerland and France (Moreau et al. 2010), while A. minutum (Bridgman and Fitch, 1894) has been obtained by E. ambiguella in France and Switzerland and by S. pilleriana in Germany (Villemant et al. 2011).

Taxonomic notes

After its introduction in Canada, A. flaveolatum was confused by some American authors (Carlson 1979, Dasch 1984) with similar Nearctic species belonging to the same genus (Barron 1989).

Parania geniculata (Holmgren, 1857)

Figure 1

Atrometus geniculatus: Silvestri 1912: 296; Stellwaag 1928: 665.

Sinophorus geniculatus: Hoffmann and Michl 2003: 3 (misinterpretation).

Italian distribution of reared parasitoids

Trentino-South Tyrol: Silvestri 1912.

Distribution

This species is widespread over most of the temperate Holarctic region. It is quite common in the Nearctics (Yu et al. 2012), while in the Palaearctics its distribution is limited to the Western part only: Europe, Central Russia and Turkey (Yu et al. 2012, Zwakhals and van Achterberg 2017).

Host range

Yu et al. (2012) list 38 hosts for this species, 21 of which belonging to the family Tortricidae, the remaining, in order of importance, to the families Pyralidae (4 species), Gelechiidae (3), Noctuidae (2), Choreutidae, Galacticidae, Geometridae, Lycaenidae, Nolidae, Sesiidae and Psychidae (all represented by a single species). Some economically important species are included, as the Oriental fruit moth Grapholita molesta (Busck, 1916) and the codling moth Cydia pomonella (Linnaeus, 1758), Argyrotaenia spp., Rhyacionia spp., Choristoneura spp. (Tortricidae), and the European corn borer, Ostrinia nubilalis (Hübner, 1796) (Crambidae). The report of Andricus kollari (Hartig, 1843) (Hymenoptera Cynipidae) of Fulmek (1968) as host of P. geniculata is not reliable.

In Italy, the species is reported on Paranthrene tabaniformis (Rottemburg, 1775) (Lepidoptera Sesiidae) (Dasch 1984, without indication of locality), on Gypsonoma aceriana (Duponchel, 1843) (Lepidoptera Tortricidae) (Haeselbarth 1989) and L. botrana (Silvestri 1912). The latter is not included in the list of Yu et al. (2012) and represents the only record for this species on EGVM.

Ecological role

Silvestri (1912) reared a single male of this species from overwintering pupae of EGVM in San Michele (Trentino) in May.

Taxonomic notes

Parania geniculata is one of the smallest European species of the subfamily Anomaloninae. It parasitizes mostly Tortricidae (Schnee 2008). The species was originally described by Holmgren (1857) as Anomalon geniculatum and subsequently transferred to the genus Atrometus Förster, 1869 by Thomson (1892). Silvestri (1912) has erroneously attributed the authorship of the species to Förster, who just described the genus Atrometus (Förster 1869). Then Townes (1971) transferred the species to Parania Morley, 1913, with P. geniculata as the only European species of this small, but widely distributed genus. Probably because of this nomenclatural inexactness, Hoffmann and Michl (2003) have misinterpreted the specimen obtained by Silvestri and put it in synonymy with Sinophorus geniculatus Gravenhorst, 1829, which belongs to the subfamily Campopleginae. The specimen figured by Silvestri (1912, fig. XXXIX, Figure 1A) clearly belongs to Anomaloninae. After comparing the figure by Silvestri with specimens of Atrometus insignis Förster, 1878 (a South European species that could be confused with Parania), and Parania geniculata in his collection, Heinz Schnee recognized the specimens depicted by Silvestri as P. geniculata, for the following reasons: “…small number of flagellomeres, small brachial cell, mesoscutum and scutellum somewhat longer, and slender hind tarsi”; on the contrary, “…Atrometus insignis is therefore out of the question, because in the drawing the characteristic transverse furrow on posterior part of the mesoscutum is absent and the brachial cell is too small. Also the hind tarsi of P. geniculata are much thinned, while they are strongly thickened in males of A. insignis. Moreover, the hosts of A. insignis are Zygaena spp. (Lepidoptera Zygaenidae) and other host assignments are very likely wrong (Schnee in litteris)”. We have searched for the specimen identified by Silvestri without finding it.

Figure 1. 

Parania geniculata (Holmgren, 1857), male (IT, Udine, Aug. 28, 1985, leg. Allegro ex Gypsonoma aceriana; ZSM) A drawing of male in a dorsal vision by Silvestri (1912) B habitus, lateral view C head and anterior part of thorax, dorsal view D head, frontal view E wings F head and mesosoma lateral view.

Trichomma enecator (Rossi, 1790)

Figure 2

Trichomma enecator: Colombera et al. 2001: 94; Scaramozzino et al. 2017b: 133.

Italian distribution of reared parasitoids

Piedmont: Colombera et al. 2001.

Tuscany: Scaramozzino et al. 2017b.

Distribution

Palaearctic species occurring throughout Europe, Canary Islands, Near East (Turkey and Syria), Northern and Central Russia, Kazakhstan, Russian Far East, Korea and Japan (Yu et al. 2012; Zwakhals and van Achterberg 2017). In 1931, it was released in North America (New Jersey, USA) to control the Oriental fruit moth, without becoming established (Carlson 1979).

Host range

Females lay eggs on young larvae that live hidden in the vegetation. Yu et al. (2012) list 28 host species, many of which belong to the family Tortricidae, including the fruit crop pests Cydia pomonella (Linnaeus, 1758), Archips rosana (Linnaeus, 1758) and Grapholita molesta (Busck, 1916). The following species need to be added to the list: Aphelia (Zelotherses) peramplana (Hübner, 1825) (= A. amplana Hübner, 1813) (Vas et al. 2015), Archips crataegana (Hübner, 1799) (Lungu-Constantineanu 2009), Cacoecimorpha pronubana (Hübner, 1799) (Scaramozzino et al. 2017b), Cydia pactolana (Zeller, 1840) (Jansons 2013), Eudemis profundana (Denis & Schiffermüller, 1775) (Zaemdzhikova 2017), Sparganothis pilleriana (Denis & Schiffermüller, 1775) (Habermehl 1922), Spilonota ocellana (Denis & Schiffermüller, 1775) (Nuzhna 2010) among the Tortricidae; Anacampsis populella (Clerck, 1759) (Hassanein 1978) among Gelechiidae; Macrothylacia rubi (Linnaeus, 1758) (Nuzhna 2010) among Lasiocampidae; Acrobasis suavella (Zincken, 1818) (Morley 1915) among Pyralidae; and Prismosticta fenestrata Butler, 1880 among Endromidae (Morley 1915). Habermehl (1922) reports as host also Gelechia boticella, but the identity of this species still remains unclear.

Ultimately, 40 host species of Trichomma enecator have been reported: 25 species belonging to Tortricidae, three each to Gelechiidae and Pyralidae, and one each to Elachistidae, Endromidae, Erebidae (Lymantria dispar (Linnaeus, 1758)), Gracillariidae, Lasiocampidae, Noctuidae, Nolidae and Psychidae. The record by Starke (1956 in Yu et al. 2012) of Plioreocepta poeciloptera (Schrank, 1776) (Diptera Tephritidae) seems unlikely and is probably wrong.

In Italy, T. enecator is reported on: Earias clorana (Linnaeus, 1761) (Lepidoptera Nolidae) on goat willow (Salix caprea Linnaeus, 1753) (Leonardi 1925); Cydia pomonella in Campania (Sciarra 1915) and Emilia Romagna (Faggioli 1938); Tortrix viridana Linnaeus, 1758 and Aleimma loeflingiana (Linnaeus, 1758) (Lepidoptera Tortricidae) on oak in Calabria and Campania, respectively (Silvestri 1923); Grapholita molesta in Emilia Romagna (Grandi 1937); Rhyacionia buoliana (Denis & Schiffermüller, 1775) in Tuscany (Zocchi 1952); Cacoecimorpha pronubana feeding on spurge flax (Daphne gnidium Linnaeus, 1753) in Tuscany (Scaramozzino et al. 2017b).

Ecological role

Trichomma enecator is a solitary, koinobiont, larval-pupal endoparasitoid on fruit-mining or other concealed lepidopterous larvae. It is one of the most common parasitoids of the codling moth in Europe (Franck et al. 2017). Although quite common, its control action on the codling moth is limited, with parasitization rates rarely exceeding 5% (Table 4), being inexplicably absent in some apple orchards (Maalouly et al. 2013).

Trichomma enecator (Rossi): parasitization rates recorded on Cydia pomonella and other hosts.

Species Place Parasitization rate Reference Notes
Cydia pomonella France 0.23–3.11 Rosenberg (1934) Winter generation on apple; found in 8 out of 11 locations studied
Cydia pomonella Switzerland, South-West 0.6–2.9 Athanassov et al. (1998) Winter generation on apple; T. enecator represents 42% of all the reared parasitoids
Cydia pomonella Syria, coastal region 5.64 Ismail and Albittar (2016) In a neglected apple orchards in 2003
Cydia pomonella Syria, coastal region 1.92–3.27 Ismail and Albittar (2016) In two neglected apple orchards in 2004, all generations
Cydia pomonella Germany, Baden-Württemberg 1.22 Lashkari-Bod and Zebitz (2014) On apple, from spring and autumn collections
Cydia pomonella Switzerland, South 9.9 Mills (2005) Maximum percent rates recorded in an individual orchard
Cydia pomonella Austria, East 7.4 Mills (2005) Maximum percent rates recorded in an individual orchard
Cydia pomonella Spain, Asturia 0.26–0.83 Miñarro and Dapena (2004) In 2001 and 2002 respectively; winter generation on apple
Cydia pomonella Switzerland, upper Rhine-valley parasitization rates as in Wildbolz and Staub (1985) and Athanassov et al. (1998) Höhn et al. (1999) Winter generation on apple
Archips crataegana Romania, Iaşy 9.21 Lungu-Constantineanu (2009) From oak (Quercus petraea)
Archips rosana Poland, environs of Poznań 0.48–0.28 (average of two years = 0.76) Piekarska-Boniecka (1994) On red currant in 1989 and 1990 respectively

What we know about its biology is mainly due to Rosenberg (1934), who studied the codling moth in French apple orchards. This parasitoid attacks the host larvae, hibernating in the larval stage inside the host; the adult emerges from the pupa, some weeks before the host; the emergence period, in outdoor insectary, lasts 10–24 days, from the second half of May to the beginning of June. In captivity both genders may live approximately a month. Females start to oviposit one or two days after emergence, and their eggs hatch in approximately eight days (Rosenberg 1934). Despite its presence in most of the areas in Rosenberg’s survey, the parasitism rate never surpassed 3.11%.

Trichomma enecator females parasitize all the larval instars of the codling moth inside the fruits. The females are attracted by exudates that accumulate on the surface of the fruits infested by the codling moth larvae; in the absence of these exudates, the parasitization behavior is disrupted (Mills and Dixon 1993). To breed this species in insectarium is very difficult (Mills 2005), even if Russ and Faber (1978) were able to rear it until F6 generation by the same method used to rear Ascogaster quadridentatus Wesmael, 1845 (Hymenoptera, Braconidae).

At our latitude, T. enecator is a multivoltine species, while in Central-Northern Europe (Gauld and Mitchell 1977, Sedivy 2001) and Spain (Miñarro and Dapena 2004) it is presumably bivoltine. According to our personal observations, in Italy it shows three generations per year, and can attack all three generations of EGVM.

Trichomma enecator has a secondary importance on EGVM; Telenga (1934) obtained it in early June in Crimea. In Piedmont (Italy), a single specimen emerged from pupae of the overwintering generation of L. botrana (Colombera et al. 2001). In the Natural Reserve of San Rossore (Pisa, Tuscany), we obtained 13 specimens of T. enecator from EGVM pupae in July 2012 and from EGVM and C. pronubana pupae in May and July 2014. Pupae of both tortricids were collected into the nests formed by the larva on the apical buds of the spurge flax Daphne gnidium (Malvales, Thymelaeaceae) (Scaramozzino et al. 2017b).

Figure 2. 

Trichomma enecator (Rossi, 1790) (IT, San Rossore Pisa, ex Lobesia botrana) A female habitus lateral view B male habitus lateral view C female head frontal view D female head and mesosoma dorsal view E female head and mesosoma lateral view.

Subfamily: Campopleginae

As mentioned, 27 taxa belonging to nine different genera of Campopleginae are reported on EGVM in Eurasia (Table 3). Many species of this subfamily are important natural enemies of insect pests (Lepidoptera above all) and were often used in biological control programs (Quicke 2015). The few species that have been studied in detail often represent the dominant component in parasitoid community of a given host and could be good biological control agent candidates (Jenner et al. 2005). Unfortunately, the uncertainty associated with the taxonomic status of many species and the lack of updated and well-illustrated literature often represent an obstacle to their use in biological control programs. Females are barely identifiable and males are often indeterminable (Horstmann 2012). Misidentifications are easy, making associated host ranges mostly unreliable (Fitton and Walker 1992, Shaw and Horstmann 1997, Jenner et al. 2013). It descends that it is difficult to adopt a species as a potential biological control agent, particularly focusing on the risk it could represent for non-target species in a new area. Probably, for many species the host range is narrower than that inferred from the literature (Jenner et al. 2013, Horstmann 2012).

Campoplex sp. Gravenhorst, 1829

Campoplex sp.: Pinna et al. 1989: 82; Lozzia and Rigamonti 1991: 34; Coscollá 1997: 218.

Italian distribution of reared parasitoids

Piedmont: Pinna et al. 1989; Lozzia and Rigamonti 1991.

Distribution and host range

The cosmopolitan genus Campoplex Gravenhorst, 1829 includes ca. 210 species of koinobiont endoparasitoids of microlepidopteran larvae (mainly of the Tortricidae family, but also of Coleophoridae, Gelechiidae, Pyralidae etc.), and to a lesser extent of macrolepidoptera, Hymenoptera Symphyta and few Coleoptera Curculionidae (see Yu et al. 2012 for a more comprehensive review). In Europe approximately 90 species are recorded (Zwakhals and van Achterberg 2017).

Ecological role

Pinna et al. (1989) obtained an unidentified species of Campoplex from overwintering specimens of L. botrana, with parasitism rates variable from 4.7 to 36.9%. Lozzia and Rigamonti (1991) found an unidentified species from overwintering generation of the EGVM, with a parasitism rate close to 4%.

Campoplex borealis (Zetterstedt, 1838)

Figure 3

Campoplex borealis: Nuzzaci and Triggiani 1982: 49.

Italian distribution of reared parasitoids

Apulia: Nuzzaci and Triggiani 1982 [on Daphne gnidium L.].

Distribution

The species is widely spread throughout Europe and Northern Russia (Yu et al. 2012; Zwakhals and van Achterberg 2017). In 1937, 96 adults of C. borealis were released in U.S.A. (Connecticut) from Europe, to control the European pine shoot moth, Rhyacionia buoliana (Denis & Schiffermüller, 1775) (Lepidoptera Tortricidae), but the species has not become established (Dowden 1962, Bartlett et al. 1978).

Host range

Yu et al. (2012) report 19 host species associated with C. borealis, belonging to the families Coleophoridae (8 species), Tortricidae (4 species, L. botrana is not into the list), Psychidae, Yponomeutidae, Eriocraniidae, Gelechiidae, Gracillariidae, Simaethidae (one species each) and on the weevil Anthonomus pomorum (Linnaeus, 1758) (Coleoptera Curculionidae).

Ecological role

In three years of sampling on Daphne gnidium, Nuzzaci and Triggiani (1982) obtained three specimens of this parasitoid from larvae of L. botrana (identified by K. Horstmann). This is the only record on EGVM so far.

Taxonomic notes

Campoplex borealis is the species that gives its name to a “borealis” species-group of the genus Campoplex (Horstmann 2012). With the name of C. borealis were indicated at least six different species (Horstmann 2012), morphologically very similar and mainly characterized by their host preferences. Right now, eight species are included in this species-group: C. borealis (Zetterstedt, 1838), C. jaeckhi (Bauer, 1936), C. psammae (Morley, 1915), C. punctipleuris Horstmann, 1980, C. serratellae Horstmann, 2012, C. caloptiliae Horstmann, 2013, C. tussilaginis Horstmann, 2013 and Campoplex linosyridellae Horstmann, 2016. They are mainly related to Coleophoridae and Gelechiidae; one species, C. caloptiliae, lives on Gracillariidae, while a second species close to C. psammae lives on Psychidae (Horstmann 1980, 2012, 2013, Shaw et al. 2016). Horstmann (1985) does not mention EGVM among the hosts of C. borealis, despite a male and a female collected by Nuzzaci and Triggiani are in his collection in ZSM.

Figure 3. 

Campoplex borealis (Zetterstedt, 1838) (female: SP, Barcelona, March 28, 1964; male: CH, Sustenpaß, September 10, 1989, ex Acleris variegana; ZSM) A female habitus lateral view B male habitus lateral view C female head lateral view D female head frontal view E female head dorsal view F female propodeum dorsal view G female metasoma dorsal view H opened cocoon.

Campoplex capitator Aubert, 1960

Figures 4, 5

Campoplex capitator: Marchesini and Dalla Montà 1992: 10, 1994: 205, 1998: 3; Dalla Montà et al. 1993; Coscollá 1997: 214; Colombera et al. 2001: 94; Marchesini et al. 2006: 12; Bagnoli and Lucchi 2006: 140; Marchesini 2007: 41; Lucchi and Santini 2011: 199; Loni et al. 2016: 131; Scaramozzino et al. 2017b: 132.

Campoplex difformis: Thompson 1946: 484.

Omorgus difformis Gmelin: Catoni 1910: 17, 1914: 250; Silvestri 1912: 295; Schwangart 1913: 6, 1918: 547; Ruschka and Fulmek 1915: 391; Leonardi 1925: 259; Boselli 1928: 189; Stellwaag 1928: 663.

Italian distribution of reared parasitoids

Trentino-South Tyrol: Catoni 1910, 1914; Silvestri 1912; Schwangart 1913, 1918; Ruschka and Fulmek 1915.

Veneto: Marchesini and Dalla Montà 1992, 1994, 1998; Dalla Montà et al. 1993; Marchesini et al. 2006; Marchesini 2007.

Piedmont: Colombera et al. 2001.

Tuscany: Dalla Montà et al. 1993; Bagnoli and Lucchi 2006; Lucchi and Santini 2011; Loni et al. 2016; Scaramozzino et al. 2017b.

Campania: Silvestri 1912.

Sicily: Alcamo (TP), ex Lobesia botrana on grapes (ZSM new record).

Distribution

Campoplex capitator is a Mediterranean species, occurring in the Iberian Peninsula, France, Corsica, Italy, Switzerland and Turkey (Yu et al. 2012; Zwakhals and van Achterberg 2017). It is widespread in most of the southern European wine-growing areas (Bagnoli and Lucchi 2006), although its presence on EGVM in Southern Italy was not definitely ascertained. Nuzzaci and Triggiani (1982), in Apulia, underline the presence of C. difformis on EGVM feeding on Daphne gnidium and the absence of C. capitator, as already stated by Silvestri (1912). When checking his collection in Naples, we found two series of specimens, both reported as C. difformis from L. botrana. Actually, the two series are composed of at least three different species:

1. Campoplex capitator from Portici (Naples), 5 females and 3 males, and from San Michele all’Adige (Trento), 3 females, 3 males and 1 individual without metasoma. The specimens from San Michele all’Adige have the same origin of those studied and published by Catoni (1910) with the name of C. difformis and identified by O. von Schmiedeknecht.

2. Diadegma stigmatellae Horstmann, 1980 (Campopleginae), 6 males and 4 females from Portici, a parasitoid of Gracillariidae (Shaw and Horstmann 1997).

3. Pristomerus vulnerator (Panzer, 1799) (Cremastinae) 1 male and 1 female from Portici.

We are not sure if the two series of specimens correspond to those actually studied by Silvestri but we think that the Campoplex specimens he had attributed to Omorgus difformis belong to C. capitator.

In the Horstmann collection, as well as in the general collection of ZSM, we found 7 females and 6 males of C. capitator from Sicily (Alcamo, TP), emerged from larvae of L. botrana feeding on grapes in July 2007, August 2009 and late May-June 2010. Also in the Horstmann collection we examined a male and a female of C. capitator from Piacenza (Northern Italy), obtained from E. ambiguella.

Host range

Campoplex capitator seems to have an extremely limited host range. It was discovered on EGVM for the first time by Coscollá (1980) in Spain. Yu et al. (2012) list only two host species, L. botrana and Ancylis mitterbacheriana (Denis & Schiffermüller, 1775) (Lepidoptera Tortricidae). According to Villemant et al. (2011), in French vineyards C. capitator lives mainly at the expenses of L. botrana and E. ambiguella, though it has been obtained occasionally also from S. pilleriana. All the mentioned hosts live mainly on the grapevine, with the exception of A. mitterbacheriana, an univoltine leaf folder which lives on deciduous woodlands and whose larvae feed on the leaves of beech, common hornbeam, oaks, and sweet chestnut (Alford 2012, Brown et al. 2008).

Ecological role

Campoplex capitator is a solitary koinobiont larval endoparasitoid. Its development is strongly synchronized with L. botrana: both species overwinter in the same places, and live in close association, the first at the expense of the larvae of all the moth generations. The female oviposits into the body of EGVM larvae of 2nd-4th instar (Thiéry 2008, Villemant et al. 2011). Endophagous larva kills the host after spinning its own cocoon inside the moth cocoon. The larva of C. capitator builds a delicate elongated semi-transparent cocoon characterized by rounded poles, white color and a thin median opaque transverse line (Figure 4D).

Figure 4. 

Campoplex capitator Aubert, 1960 (female and male: IT, San Rossore Pisa ex Lobesia botrana) A female habitus lateral view B male habitus lateral view C propodeum female, dorsal view D opened cocoon inside a EGVM cocoon, in a dried nest on Daphne gnidium E distal 24 articles of female antenna.

The parasitization rates recorded in Europe (Italy excluded) are shown in Table 5, while those recorded in Italy are shown in Table 6.

Campoplex capitator parasitization rates recorded on the European grapevine moth in Europe (Italy excluded).

Author/s and publication year Country and region Host plant or cv Year 1st generation (antophagous) 2nd generation (carpophagous) 3rd generation (carpophagous)
Carlos et al. 2006 Portugal, Douro, S. Luiz grapevine 2002 6.98% 3.88
Carlos et al. 2006 Portugal, Douro, Bonfim grapevine 2002 5.5%
Coscollá 1980 “comarcas vitícolas valencianas”* grapevine 1978 4.62%
Coscollá 1980 “comarcas vitícolas valencianas”* grapevine 1979 1.35% <0.75% 0.79%
Coscollá 1980 “comarcas vitícolas valencianas”* grapevine 1980 1% 0 0
Moreau et al. 2010 Switzerland, Yvorne (VD) Grapevine cv Chasselas 2003 1.53%
Moreau et al. 2010 Switzerland, Yvorne (VD) Cv Pinot noir 2003 3.63%
Moreau et al. 2010 Switzerland, St Pierre-de-Clages (VS) Chasselas 2003 1.12%
Moreau et al. 2010 France, Tavel (SF) Grenache 2003 17.6%
Moreau et al. 2010 France, Roquemaure (SF) Syrah 2004 0.56%

Campoplex species: percentages of parasitism on the European grapevine moth reported in Italy by different authors.

Species or Author/s and publication year Italian Region/ Locality Host plant Year 1st generation (antophagous) 2nd generation (carpophagous) 3rd generation (carpophagous)
Campoplex sp.
Pinna et al. 1989 Piedmont/ Ghemme (NO) grapevine 1986/87 2.46* does not occur
Pinna et al. 1989 Piedmont/ Piverone and Caluso (TO) grapevine 1985/86 1.78* does not occur
Pinna et al. 1989 Piedmont/ Piverone and Caluso (TO) grapevine 1986/87 13.28* does not occur
Pinna et al. 1989 Piedmont/ Riccaldone e Castelrocchero (AL) grapevine 1986/87 18.24* does not occur
Pinna et al. 1989 Piedmont/ Mango e Castellinaldo (CN) grapevine 1986/87 6.33* does not occur
Lozzia and Rigamonti 1991 Piedmont/ Ghemme (NO) grapevine 1988 12.50 does not occur
Campoplex capitator
Colombera et al. 2001 Piedmont/ Caravino (IPM) grapevine 1998 7.4* 0 does not occur
Colombera et al. 2001 Piedmont/ Caravino (IPM) grapevine 1999 3.07* 1.9* does not occur
Colombera et al. 2001 Piedmont/ Settimo Vittone (Convent.) grapevine 1998 0.61* 0 does not occur
Colombera et al. 2001 Piedmont/ Settimo Vittone (Convent.) grapevine 1999 1.85* 5.88* does not occur
Marchesini and Dalla Montà 1994 Veneto/ Pernumia (PD) grapevine 1988 1.46
Marchesini and Dalla Montà 1994 Veneto/ Pernumia (PD) grapevine 1989 12.17 3.15 9.4
Marchesini and Dalla Montà 1994 Veneto/ Pernumia (PD) grapevine 1990 11.78 0.46 0
Marchesini and Dalla Montà 1994 Veneto/ Pernumia (PD) grapevine 1992 0 0 0.02
Marchesini and Dalla Montà 1994 Veneto/ Colognola (VR) grapevine 1990 0.74 0.74 2.69
Marchesini and Dalla Montà 1994 Veneto/ Colognola (VR) grapevine 1991 0.33 0 3.52
Marchesini 2006 and 2007 Veneto grapevine 2000 (2) 3.8/14.3 6.4/8.3
Marchesini 2006 and 2007 Veneto grapevine 2001 (2) 0/6.0 13.0/10.0 0.5/2.0
Campoplex difformis
Nuzzaci and Triggiani 1982 Apulia/ Monopoli (BA) and Martinafranca (TA) Daphne gnidium 1979–82 4**

Silvestri (1912) frequently found C. capitator on EGVM, both in Trentino (Northern Italy), in spring, and in Portici (Naples), from July to September. In Veneto (Northern Italy) it attacks all the generations of EGVM, with irregular and not particularly high rate of parasitism, often less than 1%, sometimes close to 12% in the first generation and 14% in the second and slightly more than 8% in the third generation (Marchesini and Dalla Montà 1994, Marchesini et al. 2006); sometimes it is absent. In Piedmont, where EGVM developed 2 generations per year, Colombera et al. (2001) recorded parasitization rates of 7.4% and 5.9%, respectively. In Tuscany (Central Italy), on grapevine, C. capitator is the most frequent species among larval parasitoids, showing a good parasitic activity throughout the region, mostly on larvae of the first two generations of the year (Bagnoli and Lucchi 2006). In the Natural Reserve of San Rossore (Pisa, Tuscany), it is very frequent on Daphne gnidium, where it represents the dominant species in the parasitoid community of EGVM; attacking larvae of all three generations, it contributed for more than 58% of the total number of parasitoids found in 2014 and more than 73% in 2015, with an overall annual parasitization rate for 2014 next to 10% (Loni et al. 2016).

In France, the rates of parasitism can be very high, especially in the EGVM first generation (Villemant et al. 2011). In the vineyards of Valencia (Spain), C. capitator is the only larval parasitoid that plays a significant role in the control of EGVM, even if the total parasitism levels found in that region were low across all the three generations (Coscollá 1997). In Douro Wine Region (Portugal), C. capitator is the second most abundant parasitoid of EGVM (Carlos et al. 2013), representing the 11.8% of parasitoids obtained in 10-year surveys. In Turkey, the species is mostly widespread in the Aegean vineyards (Koclu et al. 2005, Özsemerci et al. 2016).

Despite being considered one of the possible candidates for use in the biological control of EGVM, the knowledge about its behavior and its development are too limited and still some difficulties have to be overcome to develop an efficient mass rearing in bio-factory (Bagnoli and Lucchi 2006). Nevertheless, a recent cooperation between Italian and Chilean entomologists seems very promising (Lucchi et al. 2017).

Taxonomic notes

Horstmann (1985) divided the Western Palaearctic species of the genus Campoplex in four species-groups: melanostictus (including the spurius-group), continuus, discrepans and difformis species-groups; later, the C. borealis species-group was added (Horstmann 2012). Both Campoplex capitator and C. difformis belong to “difformis” species-group, which is characterized by occipital carina joining hypostomal carina at a right angle at the base of the mandibles (i.e., occipital carina turned outwards ventrally); slender body with apically compressed metasoma; hind tibia with the median outer part from yellowish red to reddish brown, and basal part not clearly brightened; ovipositor sheath relatively long (at least as long as the hind tibia). Horstmann (1985) describes the female of C. capitator as follows in the key: body size approx. 5 mm, face wider than long, temples behind the eyes narrow, the lines (as seen in profile from above) touching the outside of the eyes and temples usually intersecting in or behind the scuto-scutellar groove, antennal segments, in the last quarter, at least as long as wide, prepectal carina medially not significantly broader than ventrolaterally and not clearly notched, hind coxae black with hind femora predominantly red, ovipositor sheath 1.4–1.7 times as long as the hind tibia, second metasomal segment not more than 1.6 times as long as wide.

The females of C. difformis, which are very similar to those of C. capitator, in Horstmann’s keys are distinguished by: body size approx. 8 mm, face longer than wide, antennal segments, in the last quarter, much wider than long, and the area superomedia of propodeum wide, and not clearly separated from the area petiolaris; both areas are clearly depressed.

Villemant et al. (2011) pointed out that C. capitator has often been confused with C. difformis in the past and many reports of this species on EGVM should probably be related to C. capitator. The identifications of C. difformis made by Silvestri as well as those of Catoni are to be referred to C. capitator (see above). The record of Nuzzaci and Triggiani (see C. difformis), whose specimens were identified by Horstmann, has to be considered correct.

Molecular-based studies indicate that C. capitator could be conspecific of C. formosanae Horstmann, 2012, a species reared on Enarmonia formosana in Germany (Hunt and Kuhlmann 2007, Hunt et al. 2008). The species was identified as C. dubitator at first, but then recognized as a valid species by Horstmann (2012). Despite molecular differences between the two species were not significant (Hunt and Kuhlmann 2007, Hunt et al. 2008), laboratory tests showed that C. formosanae was unable to develop on EGVM larvae and small but constant morphological characters have been found that lead to consider C. formosanae as a distinct species from C. capitator (Hunt et al. 2008, Jenner et al. 2013).

Figure 5. 

Campoplex capitator Aubert, 1960 (female: IT, San Rossore Pisa ex Lobesia botrana) A wings B head frontal view C head and mesosoma dorsal view D mesopleuron with epicnemial and postpectal carinae, ventral view.

Campoplex difformis (Gmelin, 1790)

Campoplex difformis: Nuzzaci and Triggiani 1982: 49.

Italian distribution of reared parasitoids

Apulia: Nuzzaci and Triggiani 1982 [on Daphne gnidium L.].

Distribution

The species is present throughout Europe up to the Caucasus and Uzbekistan, the Canary Islands and Madeira, Tunisia and Greenland (Yu et al. 2012; Zwakhals and van Achterberg 2017).

Host range

Yu et al. (2012) list 64 host species belonging to 18 different families (15 of Lepidoptera and 3 of Hymenoptera). This long list has to be verified, because in the past the specific interpretation of C. difformis was rather uncertain (see taxonomic notes under C. capitator and Horstmann 1985). The most represented family is that of Tortricidae, with 35 species (including L. botrana and E. ambiguella). Tortricids could be actually the only hosts of C. difformis, because all known hosts of the “difformis” species-group belong to this family (Horstmann 1985). Archips podana (Scopoli, 1763) was the only host ascertained for this species in the work of Horstmann (1985). In Evenhuis and Vlug (1983), a hypothetical Campoplex difformis, so identified by Horstmann, is reported attacking three other tortricid species, Pandemis cerasana (Hübner, 1786), Adoxophyes orana (Fischer v. Röslerstamm, 1834) and Acleris rhombana (Denis & Schiffermüller, 1775).

Ecological role

Campoplex difformis is a koinobiont larval endoparasitoid often reported as a parasitoid of E. ambiguella in France (Voukassovitch 1924). Its larva kills the moth larva when it is ready to pupate, and weaves its own cocoon next to the host spoils (Marchal 1912, Voukassovitch 1924). In Apulia (Southern Italy), this species occurred frequently, showing a parasitism rate of approx. 4% on EGVM larvae feeding on Daphne gnidium (Nuzzaci and Triggiani 1982). The species has been reported on L. botrana in Austria, France, Germany, Russia, Spain and Bulgaria, as well as in Italy (Thompson 1957, Zapryanov and Stoeva 1982, Zapryanov 1985).

Campoplex difformis is itself the victim of Dibrachys microgastri (Bouché, 1834) (Hymenoptera Pteromalidae) (Faure and Zolotarewsky 1925, Zapryanov and Stoeva 1982), Perilampus tristis Mayr, 1905 (Hymenoptera Perilampidae) (Thompson 1958) and Cirrospilus sp. (Hymenoptera Eulophidae) (Noyes 2017).

Taxonomic notes

Campoplex difformis (Gmelin) was designated as the type species of the genus Campoplex Gravenhorst, 1829 by Westwood (1840). It also gives the name to a complicated group of very similar species, with morphological characteristics insufficient to allow a definitive identification (Jenner et al. 2013). In the past this species was mainly attributed to the genera Limneria Holmgren, 1859 and Omorgus Förster, 1869 (= Omorga Thomson, 1887). Unfortunately, the interpretation of the species Ichneumon difformis Gmelin, until the studies of K. Horstmann (1969, 1985), has been uncertain. The type of Gmelin was destroyed. Then, following the first interpretation of the species given by Gravenhorst (1829), Horstmann fixed the lectotypus of Limneria mutabilis Holmgren, in Holmgren’s collection in Stockholm as a neotypus of C. difformis (Horstmann 1969, 1985). Thus, C. mutabilis of Holmgren became a junior synonym of C. difformis, and C. difformis sensu Holmgren (and Thomson) became Campoplex deficiens Gravenhorst, 1829. Therefore, the interpretation of the species given by Gravenhorst (1829) [and hence by Horstmann (1985)] differed from that of other taxonomists (mainly Holmgren, Thomson and Schmiedeknecht), who considered C. difformis and C. mutabilis two distinct species. For this reason Aubert (1971, 1974 and 1981), another leading authority in the ichneumonid taxonomy, rejected the neotypus fixed by Horstmann and created another typus in the collection of Thomson in Lund, in order to keep C. mutabilis as a separate species from C. difformis. Consequently, C. deficiens Gravenhorst became synonym of C. difformis (see Table 7). In this work we follow the interpretation of Gravenhorst (1829), Horstmann (1969, 1985), and Yu and Horstmann (1997). Campoplex difformis has three synonyms: Campoplex lineolatus Ratzeburg, 1844, Limneria mutabilis Holmgren, 1860 and Nepiera algerica Habermehl, 1922, and a variety with dark hind legs (var. obscuripes Greese, 1927).

Different interpretations and synonyms attributed by Horstmann (1969) and Aubert (1971) to the triplet C. difformis, C. mutabilis, and C. deficiens.

Species, named as in the original descriptions Interpretation given by Horstmann (1969), following Gravenhorst Interpretation given by Aubert, following Holmgren, Thomson, and Schmiedeknecht
Ichneumon difformis Gmelin, 1790 Campoplex difformis, species valida Campoplex difformis, species valida
Limneria mutabilis Holmgren, 1860 Junior synonym of Campoplex difformis Campoplex mutabilis, species valida
Campoplex deficiens Gravenhorst, 1829 Campoplex deficiens, species valida Junior synonym of Campoplex difformis

Diadegma armillata (Gravenhorst, 1829)

Figure 6

Angitia tibialis: Silvestri 1912: 296; Leonardi 1925: 259.

Angitia (Dioctes) tibialis: Stellwaag 1928: 664.

Italian distribution of reared parasitoids

Campania: Silvestri 1912.

Distribution

Diadegma armillata is a Palaearctic widespread species. It is found throughout Europe, Middle East, Caucasus, Kazakhstan, China and Korea (Yu et al. 2012; Zwakhals and van Achterberg 2017).

Host range

It is an important koinobiont larval endoparasitoid of macro- and microlepidoptera (Arctiidae, Argyresthiidae, Choreutidae, Coleophoridae, Gelechiidae, Geometridae, Gracillariidae, Lymantriidae, Noctuidae, Pieridae, Plutellidae, Psychidae, Pterophoridae, Pyralidae, Simaethidae, Tortricidae, Yponomeutidae). Yu et al. (2012) list 57 host species. Further three species have to be added to the list: Celastrina argiolus (Linnaeus, 1758) (Lycaenidae), Acrobasis marmorea (Haworth, 1811) (Pyralidae) and Swammerdamia caesiella (Hübner, 1796) (Yponomeutidae) (Shaw et al. 2016).

Diadegma armillata is particularly active against various Yponomeuta spp., attacking crop fruits, and it was introduced in 1989–1991 from France to northwestern Washington (USA), to control the apple ermine moth, Yponomeuta malinellus (Zeller, 1838) without becoming established (Unruh et al. 2003).

Ecological role

Diadegma armillata is a multivoltine species. Silvestri (1912) obtained few specimens of this wasp from EGVM cocoons in Portici (Naples). The record of Silvestri remains the only one for this species on EGVM.

Taxonomic notes

The first serious attempt to bring order in the existing confusion for the interpretation of the European species of the genus Diadegma Förster, 1869 is due to the efforts of Horstmann (1969), who revised many types of the described species. The identifications of most species were based on poor morphological characters and are unfortunately unreliable (Horstmann 1969).

Diadegma armillata belongs to the subgenus Nythobia Förster, 1869, which includes group species with the seventh metasomal tergite deeply notched medially, the ovipositor sheath longer than the first metasomal tergite and shorter than the hind tibia (Horstmann 1969). The female of D. armillata is distinguished from the related species by a head with strongly narrowed temples; last article of the antennae longer than wide; propodeum with area superomedia wider than long and opened posteriorly, costulae strong; petiolar area slightly sunken and transversely striated; first metasomal segment with slightly protruding spiracles and postpetiole with parallel sides; ovipositor sheath approx. twice the length of the first metasomal segment; front and middle coxae yellow, the middle ones sometimes darkened at the base; femora and tibiae reddish yellow; hind tibia externally dark brown with white-yellow spots at the base and in the middle; metasoma variably stained with red (Horstmann 1969).

Some doubts regarding the distribution and host range of D. armillata arises from the fact that D. semiclausum (Hellen, 1949), a common parasitoid of the diamondback moth Plutella xylostella (Linnaeus, 1758), has been misidentified with D. tibialis (Gravenhorst, 1829), which is currently a synonym of D. armillata (Horstmann 1969, Azidah et al. 2000). Under the name tibialis, D. semiclausum was introduced in 1951 from Italy to Australia to control the diamondback moth (Oatman 1978).

Figure 6. 

Diadegma armillata (Gravenhorst, 1829) (female: D, Ostfriesischen Inseln, Mollum Memmert, July 24–30, 1986, leg. V. Haeseler; male: IT, South Tyrol, Kaltern, July 29, 1959; ZSM) A female habitus lateral view B male habitus lateral view C female head dorsal view D female head frontal view E female tergites 7–9 of metasoma with ovipositor and ovipositor sheath, lateral view F female ovipositor with subapical dorsal notch lateral view.

Diadegma tenuipes (Thomson, 1887)

Angitia tenuipes: Catoni 1910: 17, 1914: 250; Schwangart 1913: 6; Boselli 1928: 189; Stellwaag 1928: 664; Thompson 1946: 483.

Italian distribution of reared parasitoids

Trentino-South Tyrol: Catoni 1910, 1914; Schwangart 1913.

Distribution

A Palaearctic species ranging from Europe up to Mongolia; in Europe it is widely present with the exception of the Iberian Peninsula, Balkans and Greece. In North Africa it is reported only from Tunisia (Yu et al. 2012; Zwakhals and van Achterberg 2017).

Host range

Diadegma tenuipes is a solitary koinobiont larval endoparasitoid of a dozen of hosts, which belong to the Lepidoptera families Coleophoridae, Momphidae, Pieridae, Plutellidae, Psychidae, Tortricidae and to the Hymenoptera families Tenthredinidae and Braconidae (Yu et al. 2012). Among these, some hosts of economic importance are indicated as the diamondback moth, the Oriental fruit moth (G. molesta), the European grape berry moth (E. ambiguella) and EGVM.

Ecological role

The only Italian records of D. tenuipes on EGVM are those of Catoni (1910 and 1914). In the vineyards of southern Romania, Bărbuceanu and Jenser (2009) found this species, along with three other species of the same genus, attacking the overwintering generation of EGVM, with a rather low parasitization rates (0.8%). In Romania it is reported by Petcu (1978) living on E. ambiguella as well.

Taxonomic notes

Like the previous species, D. tenuipes has been assigned by Horstmann (1969) to the subgenus Nythobia. It measures approx. 6 mm in length, with the head posteriorly narrowed, propodeum with evident costulae (anterior transverse carinae), and the area superomedia shorter than twice its width; areolet of the fore wing rather large and intercepted by the second recurrent vein (2m-cu) after the middle; mesopleuron with speculum almost smooth, very shiny, the area close to mesopleural suture finely dotted; the seventh metasomal tergite dorsally deeply notched, ovipositor sheath 0.8 times the length of the hind tibia and 1.4 times that of the first metasomal tergite; body black, wings with pterostigma light brown, fore coxae light, femora and tibiae reddish yellow, posterior tibiae dark behind the base and at the apex, sides of the third metasomal tergite stained with red (Horstmann 1969).

Nemeritis ssp. Holmgren, 1860

Nemeritis sp.: Del Guercio 1899: 155–156.

Italian distribution of reared parasitoids

Tuscany: Del Guercio 1899.

Taxonomic notes

The limited information provided by Del Guercio (1899) does not allow designation of the two species of Nemeritis to any of the parasitoids associated to EGVM. Though Leonardi (1925) included the work of Del Guercio in his bibliography, he did not quote these species, which are not mentioned by any other author.

The species of Nemeritis have been divided by Horstmann (1975) in four groups: caudatula- and elegans-group, which parasitizes Raphidioptera, macrocentra-group which parasitizes Coleoptera (Cleridae, Malachiidae) and Lepidoptera and lissonotoides-group for which no host records are available (Horstmann 1994). Even though most of the species seem to attack concealed hosts under the bark or in bark crevices (Horstmann 1975), few species of the macrocentra-group have been recorded on moth species of economic importance, like the Mediterranean flour moth (Ephestia kuehniella Zeller, 1879), the European grain moth (Nemapogon granella (Linnaeus, 1758)) or the strawberry fruitworm (Cnephasia longana (Haworth, 1811)) (Horstmann 1994; Yu et al. 2012).

In the past, the genus Nemeritis included species of other campoplegine genera like Campoplex, Cymodusa or Venturia (Thomson 1887, Schmiedeknecht 1909). It is possible that the two species cited as Nemeritis sp. by Del Guercio (1899) are actually Venturia canescens (Gravenhorst, 1829). Schmiedeknecht, who identified ichneumonids obtained by Del Guercio (1899, page 156), refers to Venturia canescens as Nemeritis canescens in his fundamental work on European ichneumonids (Schmiedeknecht 1909, page 1688). At least the general habitus and wing venation in the picture of the second species (Del Guercio 1899, page 156) fit with the general aspect of V. canescens.

Sinophorus crassifemur (Thomson, 1887)

Eulimneria crassifemur: Schwangart 1918: 547, Stellwaag 1928: 663.

Eulimneria ramifemur: Schwangart 1913: 6.

Italian distribution of reared parasitoids

Trentino-South Tyrol: Schwangart 1913, 1918; Stellwaag 1928.

Distribution

Transpalaeartic species widespread in Europe, present in Caucasus and Central and Far Eastern Russia as well (Yu et al. 2012; Zwakhals and van Achterberg 2017). The report for India by Morley (1913) needs to be confirmed.

Host range

Yu et al. (2012) list 14 host species for S. crassifemur, including 2 Geometridae, 2 Pieridae, 3 Pyralidae, 3 Tortricidae (Lepidoptera) and 4 species of Pamphiliidae (Hymenoptera).

Ecological role

The very little information available on this species derives from Stellwaag (1928), who reports that it has been obtained by Schwangart and Catoni in April. Nevertheless, Catoni (1910, 1914, 1915), Leonardi (1925) and Boselli (1928) do not mention this species in their lists. Thompson (1946) quotes it in Austria based on an article of Schwangart (1918) who obtained it from EGVM and E. ambiguella in Trentino. Hoffmann and Michl (2003) do not cite it. The species was also obtained from EGVM in Bulgaria (Athanassov 1981, Zapryanov 1985).

Taxonomic notes

Very likely the species referred as Eulimneria crassifemur Thomson by Schwangart (1918) and Stellwaag (1928) is Sinophorus turionum (Ratzeburg, 1844). Carlson (1979) writes: “…in literature published before the description of alkae in 1928 [Sinophorus alkae (Ellinger and Sachtleben, 1928) is a junior synonym of S. turionum] and in some literature for more than ten years thereafter, the species was misidentified as crassifemur (Thomson)”. Sanborne (1984), in his review of the world species of the genus Sinophorus Förster, 1869, indicates among the hosts of S. crassifemur, only the web-spinning larvae of Cephalcia sp. and Acantholyda sp. (Hymenoptera Pamphiliidae) on Pinus spp.

Sinophorus turionum (Ratzeburg, 1844)

Figure 7

Eulimneria alkae: Thompson 1946: 484.

Italian distribution of reared parasitoids

The indication of this species on EGVM is due to Thompson (1946) that found it in a compendium of Hymenoptera parasitoids of European corn borer of Chu and Hsia (1937) that, unfortunately, we were not able to examine. Thompson and Parker (1928), on the basis of a record by Paillot (1924), report this species under the name of Eulimneria crassifemur Thomson, both on L. botrana and on E. ambiguella.

Distribution

The species is widely distributed throughout the Palearctic region, except North Africa (Yu et al. 2012). It has been introduced several times in the United States and Canada for the biological control of the European corn borer O. nubilalis (Bartlett et al. 1978, Carlson 1979) and the pine shoot borer, R. buoliana (Syme 1971, 1984, Carlson 1979) without being established (Sanborne 1984). Its presence in the Oriental region (India and Sri Lanka) (Townes et al. 1965, Yu and Horstmann 1997) has to be confirmed.

Host range

Yu et al. (2012) list 26 host species, belonging to nine families of Lepidoptera and one family of Hymenoptera. Tortricidae and Pyraloidea are the most represented. Five other lepidopteran host species need to be added: Anania hortulata (Linnaeus, 1758), Nascia cilialis (Hübner, 1796), Pyrausta aurata (Scopoli, 1763) (Crambidae), Gymnoscelis rufifasciata (Haworth, 1809) (Geometridae) and Acrobasis advenella (Zincken, 1818) (Pyralidae) (Shaw et al. 2016).

Ecological role

It is reported as one of the main parasitoids of the European corn borer in Europe (Thompson and Parker 1928) under the name Eulimneria crassifemur, and in the Northern part of Far East (Manchuria and North Korea) (Clark 1934) as Eulimneria alkae. In the case of L. botrana, it is certainly an occasional parasitoid of minor importance, perhaps a secondary adaptation to a host different from the usual ones. In the literature we found, besides those mentioned for Italy, scattered reports of his presence on EGVM, mostly under the name crassifemur in its various generic combinations: in Austria (Thompson and Parker 1930), France (Paillot 1924, Thompson and Parker 1928), Bulgaria (Athanassov 1981, Zapryanov 1985), Germany (Thompson 1946) and Spain (Thompson 1946, Coscollá 1997). Another species, S. costalis (Thomson, 1887), has been recorded on EGVM in Moldavian vineyards, Romania (Pisicá and Páişescu-Bărbuceanu 2002, Bărbuceanu and Jenser 2009).

Taxonomic notes

Many authors dealt with this species, especially in relation to its main hosts, O. nubilalis and R. buoliana. The species has been often confused with Limnerium crassifemur (recte Sinophorus crassifemur) (Paillot 1924, Thompson and Parker 1928, Goidanich 1931, Carlson 1979), which, instead, is mainly related to species of the family Pamphiliidae (Hymenoptera) (Sanborne 1984; see notes on previous species). The name crassifemur was later corrected in alkae by Ellinger and Sachtleben (1928), which then turned out to be a synonym of Sinophorus turionum (Sanborne 1984). It is likely that the report of Thompson (1946) for Italy on EGVM, quoted by Schwangart (1918) and Stellwaag (1928), concerns the previous species (see above).

Figure 7. 

Sinophorus turionum (Ratzeburg, 1844) (female and male: IT, Lavariano, Udine, August 29, 1983 and September 26, 1983, ex Ostrinia nubilalis, ZSM) A, B female habitus lateral and dorsal view, respectively C, D male habitus lateral and dorsal view, respectively E female head dorsal view F female head frontal view G female propodeum dorsal view.

Tranosemella praerogator (Linnaeus, 1758)

Figure 8

Tranosemella praerogator: Dalla Montà et al. 1993; Marchesini and Dalla Montà 1994: 205, 1998: 3; Coscollá 1997: 215; Colombera et al. 2001: 94; Marchesini et al. 2006: 12; Marchesini 2007: 41, 48.

Italian distribution of reared parasitoids

Veneto: Dalla Montà et al. 1993; Marchesini and Dalla Montà 1994, 1998; Marchesini et al. 2006; Marchesini 2007.

Piedmont: Colombera et al. 2001.

Distribution

Holarctic widespread species (Iceland, Europe, Egypt, Central Russia and the Far East, Japan, Canada, United States) (Yu et al. 2012). Its presence in India (Morley 1913) has to be confirmed, since it is most probably based on a misidentification for a Tryphoninae Ichneumonid species belonging to the genus Dyspetes Förster, 1869 (see taxonomic notes).

Host range

Yu et al. (2012) list 44 species of Lepidoptera hosts, especially Tortricidae (32 species), including various species of the genera Archips, Argyrotaenia, Choristoneura and Pandemis. The list reports also Plutellidae, including P. xylostella, Gelechiidae as Pectinophora gossypiella (Saunders, 1844), Yponomeutidae, Sesiidae, Pyralidae, Arctiidae, Geometridae and Noctuidae.

Ecological role

In Italy, it has been reported on grapevine in Veneto and Piedmont. In Veneto (Marchesini and Dalla Montà 1994) it was regularly obtained from EGVM larvae of first and second generation, with rates of parasitism higher than those of C. capitator (Table 8). It has never been collected in the EGVM third generation, and it is supposed to overwinter on alternative hosts. In contrast, Colombera et al. (2001) found it in the first generation, with low levels of parasitization (lower than 1%), while C. capitator showed a more important and incisive activity. In Veneto, the species was hyperparasitized by Elasmus steffani Viggiani, 1967 (Hymenoptera Elasmidae), in turn attacked by Baryscapus nigroviolaceus (Nees, 1834) (Hymenoptera Eulophidae) and by an unidentified Pteromalus (Hymenoptera Pteromalidae) (Marchesini and Dalla Montà 1994). Villemant et al. (2011) assert that in some viticultural areas of France, T. praerogator mainly develops at the expense of S. pilleriana, while in other areas it may develop even at the expense of EGVM, E. ambiguella and Argyrotaenia ljungiana (Thunberg, 1797) (= pulchellana Haworth, 1811).

Tranosemella praerogator (Linnaeus): percentages of parasitism on the European grapevine moth reported in Italy by different authors.

Author/s and publication year Italian Region/ Locality Year 1st generation (antophagous) 2nd generation (carpophagous) 3rd generation (carpophagous)
Marchesini and Dalla Montà 1994 Veneto/ Pernumia (PD) 1988 0
Marchesini and Dalla Montà 1994 Veneto/ Pernumia (PD) 1989 8.7 0.35 0
Marchesini and Dalla Montà 1994 Veneto/ Pernumia (PD) 1990 9.8 4.13 0
Marchesini and Dalla Montà 1994 Veneto/ Pernumia (PD) 1991 23.76 5.37 0
Marchesini and Dalla Montà 1994 Veneto/ Pernumia (PD) 1992 5.23 0.19 0
Marchesini and Dalla Montà 1994 Veneto/ Colognola (VR) 1989 0
Marchesini and Dalla Montà 1994 Veneto/ Colognola (VR) 1990 30.4 20.9 0
Marchesini and Dalla Montà 1994 Veneto/ Colognola (VR) 1991 15.56 2.08 0
Marchesini and Dalla Montà 1994 Veneto/ Colognola (VR) 1992 17.3 4.83 0
Marchesini and Dalla Montà 1994; Marchesini 2007 Veneto/ Valpolicella (VR) 1992 (1) 17.3/6.52 4.83/0 0/0
Marchesini 2006 and 2007 Veneto 2000 (2) 1.3/0.6 0/0
Colombera et al. 2001 Piedmont/ Caravino IPM 1998 0 0 does not occur
Colombera et al. 2001 Piedmont/ Caravino IPM 1999 0.87* 0 does not occur
Colombera et al. 2001 Piedmont/Settimo Vittone 1998 0 0 does not occur
Colombera et al. 2001 Piedmont/Settimo Vittone 1999 0.31* 0 does not occur

Taxonomic notes

As already mentioned by some authors (Roman 1932, Yu and Horstmann 1997, Horstmann 2006), the name “praerogator” Linnaeus has been used in the past to indicate Dyspetes Förster 1869 [Dyspetes praerogator Thomson, 1883 unavailable name for D. luteomarginatus Habermehl, 1925] (Ichneumonidae Tryphoninae). Gravenhorst (1829) attributed the Linnean species to the genus Tryphon, perhaps following the indication of Fabricius (1804), who assigned it to the genus Bassus. Roman (1932), studying the types of Linnaeus, assigned the species to the genus Angitia Holmgren, 1859, hypothesizing the synonymy with Angitia armillata (Gravenhorst) [recte Diadegma armillata (Gravenhorst, 1829)]. Horstmann (1973) initially assigned this species to the genus Diadegma, while Townes (1971) included it in the related genus Tranosema Förster, 1869. Later, Horstmann (1978) moved the species to the genus Tranosemella Horstmann.

Figure 8. 

Tranosemella praerogator (Linnaeus, 1758) (Female: Hallig Oland, August 13–September 9, 1964, ex Clepsis spectrana Treitschke; male: D, Ostfriesischen Inseln, Mollum Memmert, July 27–August 3, 1985, leg. V. Haeseler; ZSM). A female habitus lateral view B male habitus lateral view C female propodeum and metasoma dorsal view D male head dorsal view E cells and veins of half proximal part of hind wing of female F female propodeum dorsal view.

Venturia canescens (Gravenhorst, 1829)

Venturia canescens: Marchesini and Dalla Montà 1994: 205, 1998: 3.

Italian distribution of reared parasitoids

Veneto: Marchesini and Dalla Montà 1994, 1998.

Distribution

The genus Venturia Schrottky, 1902 is represented by 136 species (Yu et al. 2012), five of which are present in Europe (Zwakhals and van Achterberg 2017). Venturia canescens is considered a cosmopolitan species, its distribution being related to grain trade and other stored products. In temperate and tropic areas around the world, it is most often found in buildings where grains or flour are stored (Carlson 1979).

Host range

Venturia canescens is a koinobiont endoparasitoid that lives on larvae of various Lepidopteran species feeding on stored goods, such as Ephestia kuehniella (Zeller, 1879), Plodia interpunctella (Hübner, 1813), Cadra spp. Walker, Apomyelois ceratoniae (Zeller, 1839), Galleria mellonella (Linnaeus, 1758) and Ostrinia nubilalis (Hübner, 1796) (Pyralidae), Nemapogon granella (Linnaeus, 1758) (Tineidae), Phthorimaea operculella (Zeller, 1873) (Gelechiidae), Prays citri Millière, 1873 (Yponomeutidae), Grapholita funebrana (Treitschke, 1835) (Tortricidae) and some Noctuidae, for a total of 22 host species (Yu et al. 2012).

Ecological role

Venturia canescens was first found associated to L. botrana in Veneto by Marchesini and Dalla Montà (1994), who obtained few specimens from the third generation larvae. Thiéry et al. (2001) recorded this species in the Bordeaux region, where females attack the mature caterpillar of EGVM and the larva weaves its pupal cocoon inside or outside of the host’s larval skin (Villemant et al. 2011). A Venturia sp. also emerged for 3rd generation larvae of L. botrana in the Aegean Region of Turkey (Koclu et al. 2005). It is considered an occasional parasitoid of L. botrana, of rather marginal importance (Villemant et al. 2011). Biological, ethological, and morphological information about this species have been provided by Frilli (1965) under the name of Devorgilla canescens.

Taxonomic notes

This species, very common and with a very wide geographical distribution, has been repeatedly described with different names and assigned to different genera. The list of synonymies and generic combinations is very long and can be found in Frilli (1965), Carlson (1979), Yu and Horstmann (1997), and Yu et al. (2012).

Conclusions

In this paper the records of ichneumonid parasitoids of EGVM were analyzed, belonging to the subfamilies Anomaloninae and Campopleginae. This is the first contribution on the ichneumonids associated with this pest in Italy.

Unfortunately, relatively little is known on the biology of most parasitoid species and, frequently, compilations of host-parasitoid records in literature are full of misinformations or taxonomic errors (Shaw et al. 2009). The lack of rearing protocols and/or the low accuracy in selection and managing the rearing substrates, often led to erroneous association of a parasitoid with a given host (Shaw 2017). Moreover, the endless changes occurring in taxonomy often require a critical interpretation of the names found in the literature.

Amongst the 14 taxa of ichneumonids cited in this paper, Campoplex capitator seems to be the best candidate to use in biological control programs against EGVM. Unfortunately, the knowledge on its behaviour and development is still not sufficient for efficient mass rearing of C. capitator in a bio-factory (Bagnoli and Lucchi 2006), though a recent cooperation between Italian and Chilean entomologists is promising (Lucchi et al. 2017).

So far, the host range of C. capitator is limited to few tortricids feeding on grapevine (Villemant et al. 2011, Yu et al. 2012), with the only exception represented by Ancylis mitterbacheriana (Aubert 1983). The life cicle of C. capitator is strongly synchronized with EGVM, with 2 to 4 generations per year moving southwards in Italy, and displaying often high parasitization rates (Tables 5 and 6).

The unsolved taxonomic confusion for the species of the genus Campoplex may still prevent their use in biocontrol programs and may represent an obstacle for those who are not confident with taxonomic interpretations and changes occurred in the group.

For this reason, we started to carry out a critical analysis of existing literature, conducting a direct check of voucher specimens preserved in historical collections with the aim to draw attention to possible taxonomic errors and false parasitoid-host relationships.

Acknowledgments

Our deep gratitude to Dr. Heinz Schnee (Markkleeberg, Germany) for valuable clarifications on Parania geniculata; Prof. Francesco Pennacchio and Dr. Bruno Espinosa (Laboratorio di Entomologia “E. Tremblay”, Department of Agriculture, University of Naples, Italy) for allowing the consultation of the materials collected by Filippo Silvestri and kept in the collection of their Institution; Dr. Stefan Schmidt (Zoologische Staatssammlung, Hymenoptera Section, Münich, Germany) and Dr. Anne Freitag (Musée Cantonal, Lausanne, Switzerland) for loans of specimens of the collection Horstmann and Aubert respectively; Mrs. Rosanna Bertozzi (Library of the Department of Agriculture, Food and Environment, University of Pisa, Italy), Prof. Giovanni Burgio (Department of Agro-Food Science and Technology, University of Bologna, Italy), Dr. Ulrich Kuhlmann, Dr. Wade Jenner and Dr. Gitta Grosskopf-Lachat (CABI, Delémont, Switzerland) for help in bibliographic research. We are also very grateful to Dr. Claire Villemant (Paris, France), Dr. Kees Zwakhals (Arkel, Netherlands), and Dr. Kees van Achterberg (Leiden, Netherlands) for their valuable and appreciated comments on the manuscript.

References

  • Alford DV (2012) Pests of ornamental trees, shrubs and flowers. A colour handbook. Second Edition. Manson Publishing Ltd, London, 480 pp. https://doi.org/10.1201/b15136
  • Athanassov AZ (1981) Studies on the parasitizing species of the family Ichneumonidae (Hymenoptera) from Bulgaria. Acta Zoologica Bulgarica 18: 87–89.
  • Athanassov AZ, Jeanneret P, Charmillot PJ (1998) Parasitoids of codling moth and other leafrollers (Lepidoptera, Tortricidae) in apple orchards and forests in south-west Switzerland. Mitteilungen der Schweizerischen Entomologischen Gesellschaft 71(1–2): 153–162.
  • Aubert J-F (1971) Les Ichneumonides du rivage méditerranéen français [Hym.] (11a série). Bulletin de la Société entomologique de France 76: 210–221.
  • Aubert J-F (1974) Ichneumonides pétiolées inédites avec un genre nouveau. Bulletin de la Société entomologique de Mulhouse (October-December 1974): 53–60.
  • Aubert J-F (1981) Syllogismes, illogismes et innovations chez les Ichneumonides. Bulletin de la Société entomologique de Mulhouse (April-June 1981): 17–22.
  • Aubert J-F (1983) Ichneumonides parasites de Coléophoride et quelques autres microlépidoptères au Musée de Verone. Bollettino del Museo Civico di Storia Naturale di Verona 9: 9–16.
  • Azidah AA, Fitton MG, Quicke DLJ (2000) Identification of the Diadegma species (Hymenoptera: Ichneumonidae, Campopleginae) attacking the diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). Bulletin of Entomological Research 90(5): 375–389. DOI: 10.1017/S0007485300000511
  • Bagnoli B, Lucchi A (2006) Parasitoids of Lobesia botrana (Den. & Schiff.) in Tuscany. Integrated Protection and Production in Viticulture, IOBC/WPRS Bulletin 29(11): 139–142.
  • Bărbuceanu D, Jenser G (2009) The parasitoid complex of Lobesia botrana (Denis et Schiffermüller) (Lep.: Tortricidae) in some vineyards of Southern Romania. Acta Phytopathologica et Entomologica Hungarica 44(1): 177–184. https://doi.org/10.1556/APhyt.44.2009.1.19
  • Barron JR (1989) Status of the parasite Agrypon flaveolatum (Gravenhorst) (Hymenoptera, Ichneumonidae), introduced to control the winter moth in Nova Scotia and British Columbia. The Canadian Entomologist 121(1): 11–26. https://doi.org/10.4039/Ent12111-1
  • Bartlett BR, Clausen CP, DeBach P, Goeden RD, Legner EF, McMurtry JA, Oatman ER (1978) Introduced parasites and predators of arthropod pests and weeds: a world review. Agriculture Handbook n.480. Agricultural Research Service, United States Department of Agriculture, US, 545 pp.
  • Boselli F (1928) Elenco delle specie d’insetti dannosi e loro parassiti ricordati in Italia dal 1911 al 1925. Laboratorio di Entomologia Agraria, Reale Istituto Superiore Agrario, Portici, 265 pp.
  • Carlos CR, Costa JR, Tão CB, Alves F, Torres LM (2006) Parasitismo asociado a la polilla del racimo de la vid, Lobesia botrana (Dennis & Schiffermüller) en la Região Demarcada do Douro. Boletín de Sanidad Vegetal-Plagas 32: 355–362.
  • Carlos C, Gonçalves F, Sousa S, Salvação J, Sharma L, Soares R, Manso J, Nóbrega M, Lopes A, Soares S, Aranha J, Villemant C, Marques G, Torres L (2013) Environmental safe strategies to control the European grapevine moth, Lobesia botrana (Den. & Schiff.), in the Douro demarcated region. Ciência e Técnica Vitivinícola 28: 1006–1011.
  • Carlson RW (1979) Family Ichneumonidae. Stephanidae. In: Krombein KV, Hurd Jr PD, Smith DR, Burks BD (eds) Catalog of Hymenoptera in America north of Mexico. Smithsonian Institution Press Washington, 315–741.
  • Catoni G (1910) Contributo per un metodo pratico di difesa contro le tiguole dell’uva. Extracts from “Il Coltivatore” 56 (13/14/18), C. Cassone, Casale Monferrato, 27 pp.
  • Catoni G (1915) Le tignole dell’uva e i loro nemici naturali nel Tirolo del sud. Rivista di Viticoltura e di Enologia Agraria, Conegliano 21(7/8): 156–160, 177–181.
  • Chu JT, Hsia SH (1937) A list of the known hymenopterous parasites of the European corn borer (Pyrausta nubilalis Huebner). Entomology & Phytopathology 5(8): 136–147. [abstract in: The Review of Applied Entomology, Series A: Agricultural 25(1937): 508.]
  • Clark CA (1934) The European corn borer and its controlling factors in the Orient. U.S. Dept. of Agriculture Technical Bulletin 455: 1–37.
  • Colombera S, Alma A, Arzone A (2001) Comparison between the parasitoids of Lobesia botrana and Eupoecilia ambiguella in conventional and integrated vineyards. IOBC/WPRS Bulletin 24(7): 91–96.
  • Coscollá R (1980) Aproximación al estudio del parasitismo natural sobre Lobesia botrana Den. y Schiff. en las comarcas vitícolas Valencianas. Boletín de Sanidad Vegetal – Plagas 6: 5–15.
  • Coscollá R (1997) La polilla del racimo de la vid (Lobesia botrana Den. y Schiff.). Generalitat Valenciana, Consejerfa de Agricultura, Pesca y Alimentación, Valencia, Spain, 613 pp.
  • Dalla Montà L, Marchesini E, Bagnoli B, Goggioli D (1993) Observations sur les ennemis naturels du ver de la grappe Lobesia botrana (Den. et Schiff.) en Vénétie et en Toscane. Meeting of the IOBC/WPRS Working Group “Integrated control in viticulture”, Bordeaux, France, 2–5 March 1993 (abstract).
  • Dasch CE (1984) Ichneumon-flies of America north of Mexico: 9. Subfamilies Theriinae and Anomaloninae. Memoirs of the American Entomological Institute 36: 1–610.
  • de Jong Y, Verbeek M, Michelsen V, de Place Bjørn P, Los W, Steeman F, Bailly N, Basire C, Chylarecki P, Stloukal E, Hagedron G, Wetzel FT, Glöckler F, Kroupa A, Korb G, Hoffmann A, Häuser C, Kohlbecker A, Müller A, Güntsch A, Stoev P, Penev L (2014) Fauna Europaea – all European animal species on the web. Biodiversity Data Journal 2: e4034. https://doi.org/10.3897/BDJ.2.e4034
  • Del Guercio G (1899) Delle tortrici della fauna italiana specialmente nocive alle piante coltivate. Nuove relazioni intorno ai lavori della R. Stazione di Entomologia Agraria di Firenze, serie prima: 117–193.
  • Delrio G, Luciano P, Prota R (1987) Researches on grape-vine moths in Sardinia. In: Cavalloro R (Ed.) Integrated pest control in viticulture. Proceedings of a meeting of the EC Experts' Group, Portoferraio, 26–28 September 1985. Balkema, Rotterdam, 57–67.
  • Dowden PB (1962) Parasites and predators of forest insects liberated in the United States through 1960. United States Department of Agriculture, Agricultural Handbook 226, 70 pp.
  • Ellinger T, Sachtleben H (1928) Notes on the central European parasites of Pyrausta nubilalis Hb. International Corn Borer Investigations Scientific Report, Chicago, 1927–1928: 109–134.
  • Evenhuis HH, Vlug HJ (1983) The hymenopterous parasites of leaf-feeding apple tortricids (Lepidoptera, Tortricidae) in Netherlands. Tijdschrift voor Entomologie 126: 109–135.
  • Fabricius JC (1804) Systema Piezatorum: secundum ordines, genera, species, adjectis synonymis, locis, observationibus, descriptionibus. Carolum Reichard, Brunsvigae, 439 + 32 pp.
  • Faggioli D (1938) Appunti entomologici. V. Bollettino dell’Istituto di Entomologia della Universita degli Studi di Bologna 11: 19–40.
  • Faure J-C (1925) Contribution à l'étude des Hyménoptères parasites. Deuxième Note: Liste des Hyménoptères parasites de Polychrosis botrana Schiff. obtenus de 1923 à 1925 en Bourgogne et dans le Sud-Est. Revue de pathologie végétale et d'entomologie agricole 12(4): 297–299.
  • Faure J-C, Zolotarewsky B (1925) Contribution à l’étude biologique de Dibrachys boucheanus Ratz. Revue de Pathologie Vegetale et d’Entomologie Agricole de France 12: 144–161.
  • Feytaud J (1913) Les ennemis naturels des insectes ampélophages. Revue de viticulture (1913): 1–24.
  • Fitton M, Walker A (1992) Hymenopterous parasitoids associated with diamondback moth: the taxonomic dilemma. In: Talekar NS (ed) , Diamondback moth and other crucifer pests. AVRDC, Taipei, 225–232.
  • Forti D (1991) Résultats préliminaires sur l'activité des parasites du ver de la grappe (Lobesia botrana Schiff.) dans le Trentino. Bulletin OILB/SROP 1992/XV, 2: 9.
  • Förster A (1869) Synopsis der Familien und Gattungen der Ichneumonen. Verhandlungen des Naturhistorischen Vereins der Preussischen Rheinlande und Westfalens 25: 135–221.
  • Franck P, Maalouly-Matar M, Olivares J (2017) Molecular tools for the detection and the identification of Hymenoptera parasitoids in tortricid fruit pests. International Journal of Molecular Sciences 18: 1–16. https://doi.org/10.3390/ijms18102031
  • Frilli F (1965) Studi sugli Imenotteri Icneumonidi 1. Devorgilla canescens (Grav.). Entomologica 1: 119–208.
  • Fulmek L (1968) Parasitinsekten der Insektengallen Europas. Beiträge zur Entomologie 18 (7/8): 719–952.
  • Gauld ID, Mitchell PA (1977) Handbooks for the identification of British insects. Vol.VII. Part 2 (b). Ichneumonidae. Orthopelmatinae & Anomaloninae. Royal Entomological Society of London, 32 pp.
  • Goidanich A (1931) Gli insetti predatori e parassiti della Pyrausta nubilalis Hübn. Bollettino del Laboratorio di Entomologia del R. Istituto Superiore Agrario di Bologna 4: 77–217.
  • Grandi G (1937) Parassiti della Cydia molesta Busck riscontrati nell’Emilia. Bolletino dell’Istituto di Entomologia della Reale Università di Bologna 9: 250–252.
  • Gravenhorst JLC (1829) Ichneumonologia Europaea. Pars II. Vratislaviae, 989 pp.
  • Habermehl H (1922) Beiträge zur Kenntnis der palaearktischen Ichneumonidenfauna. Konowia 1: 77–86.
  • Haeselbarth E (1989) Determination list of entomophagous insects. 11. IOBC/WPRS Bulletin 12(7): 1–63.
  • Hassanein FA (1978) Zur Morphologie, Biologie und Oekologie von Anacampsis populella (Clerck) (Lep., Gelechiidae). Anzeiger fuer Schaedlingskunde, Pflanzenschutz Umweltschutz 51: 20–23. https://doi.org/10.1007/BF01903247
  • Höhn H, Graf B, Höpli HU (1999) Codling moth (Cydia pomonella L.): investigations on diapause and hibernation. IOBC/WPRS Bulletin 22(6): 87–93.
  • Hoffmann C, Michl G (2003) Parasitoide von Traubenwicklern – ein Werkzeug der naturlichen Schadlingsregulation? Deutsches Weinbaujahrbuch 55: 1–13.
  • Holmgren AE (1857) Ophionslägtet Anomalon. Öfversigt at Kongliga Vetenskaps. Akademiens Förhanglingar 14: 157–186.
  • Horstmann K (1969) Bemerkungen über die Typusarten von vier Gattungen der Ichneumonidae (Hymenoptera). Opuscula Zoologica 102(1968): 1–4.
  • Horstmann K (1973) Nachtrag zur Revision der europäischen Diadegma-Arten (Hymenoptera: Ichneumonidae). Beiträge zur Entomologie 23: 131–150.
  • Horstmann K (1975) Neubearbeitung der Gattung Nemeritis Holmgren (Hymenoptera, Ichneumonidae). Polskie Pismo Entomologiczne 45: 251–265.
  • Horstmann K (1978) Bemerkungen zur Systematik einiger Gattungen der Campopleginae. Mitteilungen der Münchener Entomologischen Gesellschaft 67: 65–83.
  • Horstmann K (1980) Neue westpaläarktische Campopleginen-Arten (Hymenoptera, Ichneumonidae). Mitteilungen der Münchner Entomologischen Gesellschaft 69: 117–132.
  • Horstmann K (1985) Revision der mit difformis (Gmelin, 1790) verwandten westpaläarktischen Arten der Gattung Campoplex Gravenhorst, 1829 (Hymenoptera, Ichneumonidae). Entomofauna 6(12): 129–163.
  • Horstmann K (1994) Nachtrag zur Revision der westpaläarktischen Nemeritis-Arten (Hymenoptera, Ichneumonidae, Campopleginae). Mitteilungen der Münchner Entomologischen Gesellschaft 84: 79–90.
  • Horstmann K (2006) Revisionen von Schlupfwespen-Arten IX (Hymenoptera, Ichneumonidae). Mitteilungen der Münchner Entomologischen Gesellschaft 95: 75–86.
  • Horstmann K (2012) Revisionen von Schlupfwespen-Arten XVI (Hymenoptera: Ichneumonidae). Mitteilungen der Münchner Entomologischen Gesellschaft 102: 105–115.
  • Horstmann K (2013) Revisionen der Schlupfwespen-Arten XVII (Hymenoptera: Ichneumonidae). Mitteilungen der Münchner Entomologischen Gesellschaft 103: 113–126.
  • Hunt E, Kuhlmann U (2007) Biological control of cherry bark tortrix, Enarmonia formosana. Annual Report 2006/2007. Unpublished Report, CABI Europe - Switzerland, Delémont, Switzerland, 18 pp.
  • Hunt E, Haye T, Kuhlmann U (2008) Biological control of cherry bark tortrix, Enarmonia formosana. Annual Report 2007/2008. Unpublished Report, CABI Europe - Switzerland, Delémont, Switzerland, 12 pp.
  • Ismail M, Albittar L (2016) Mortality factors affecting immature stages of codling moth, Cydia pomonella (Lepidoptera: Tortricidae), and the impact of parasitoid complex. Biocontrol Science and Technology 26(1): 72–85. https://doi.org/10.1080/09583157.2015.1076378
  • Jenner WH, Kuhlmann U, Cossentine JE, Roitberg BD (2005) Reproductive biology and small-scale rearing of cherry bark tortrix and its candidate biological control agent. Journal of Applied Entomology 129(8): 437–442. https://doi.org/10.1111/j.1439-0418.2005.00984.
  • Jenner WH, Jenner EJ, Kuhlmann U, Bennett AM, Cossentine JE (2013) Enarmonia formosana Scopoli, cherry bark tortrix (Lepidoptera: Tortricidae). In: Mason PG, Gillespie DR. Biological control programmes in Canada, 2001-2012, CABI: 156–163.
  • Koclu T, Altindisli FO, Ozsemerci F (2005) The parasitoids of the European grapevine moth (Lobesia botrana Den.-Schiff.) and predators in the mating disruption-treated vineyards in Turkey integrated fruit protection in fruit crops. IOBC/WPRS Bulletin 28: 293–297.
  • Lashkari-Bod A, Zebitz CPW (2014) Diversity and abundance of parasitoids in organic apple orchards in Baden-Württemberg. 16th International Conference on Organic Fruit-Growing, At Stuttgart-Hohenheim, Germany: 195–199.
  • Leonardi G (1925) Elenco delle specie di Insetti dannosi e dei loro parassiti ricordati in Italia fino all’anno 1911. Parte II. Ord. Lepidoptera. Annali della Scuola superiore di Agricoltura di Portici 19/20: 81–301.
  • Loni A, Samartsev KG, Scaramozzino PL, Belokobylskij SA, Lucchi A (2016) Braconinae parasitoids (Hymenoptera, Braconidae) emerged from larvae of Lobesia botrana (Denis & Schiffermüller) (Lepidoptera, Tortricidae) feeding on Daphne gnidium L. ZooKeys 587: 125–150. https://doi.org/10.3897/zookeys.587.8478
  • Lotfalizadeh H, Masnadi-Yazdinejad A, Saber M (2012) New records of the grape berry moth hymenopterous parasitoids in Iran. Munis Entomology & Zoology 7(1): 284–291.
  • Lozzia GC, Rigamonti IE (1991) Osservazioni sulle strategie di controllo biologiche e integrate delle tignole della vite in Italia settentrionale. Vignevini 11: 33–37.
  • Lucchi A, Santini L (2011) Life history of Lobesia botrana on Daphne gnidium in a Natural Park of Tuscany. Integrated Protection and Production in Viticulture, Integrated Protection and Production in Viticulture, IOBC/WPRS Bulletin 67: 197–202.
  • Lucchi A, Ricciardi R, Loni A, Cosci F, Alvarez AR, Beeche M, Scaramozzino PL (2017) Rearing Campoplex capitator Aubert in Italy and in Chile: preliminary achievements. Future IPM 3.0 towards a sustainable agriculture, IOBC/WPRS general assembly, 15–20 October 2017, Riva del Garda, Italy, p 370.
  • Luciano P, Delrio G, Prota R (1988) Osservazioni sulle popolazioni di Lobesia botrana (Den. & Schiff.) su Daphne gnidium L. in Sardegna. Atti XV Congresso Nazionale Italiano di Entomologia, L'Aquila 1988: 543–548.
  • Lungu-Constantineanu CS (2009) Parasitoid ichneumonids (Hymenoptera) of some defoliator Tortricidae moths in Bârnova forest massif, Iaşi county. Buletinul de informare entomologicӑ, Societatea Lepidopterologicӑ Românӑ 20: 39–42.
  • Maalouly M, Franck P, Bouvier J-C, Toubon J-F, Lavigne C (2013) Codling moth parasitism is affected by semi-natural habitats and agricultural practices at orchard and landscape levels. Agriculture Ecosystems & Environment 169: 33–42. https://doi.org/10.1016/j.agee.2013.02.008
  • Marchal P (1912) Rapport sur les travaux accomplis par la Mission d’études de la Cochylis e de l’Eudémie. Librairie Polytechnique, Paris et Liege, 326 pp.
  • Marchesini E (2006) I limitatori naturali delle tignole dell’uva nell'agro-ecosistema vigneto. Vitebio, relazione 10, 6 pp.
  • Marchesini E (2007) I limitatori naturali della tignoletta nell’agroecosistema vigneto. In: Anfora G, Angeli G, Baldessari M (eds) Le tignole della vite. Agricoltura Integrata, Istituto Agrario di San Michele dell’Adige, 40–55.
  • Marchesini E, Dalla Montà L (1992) Observations sur les facteurs limitants naturels des vers de la grappe. IOBC/WPRS Bulletin 15 (2): 10.
  • Marchesini E, Dalla Montà L (1994) Observations on natural enemies of Lobesia botrana (Den. et Schiff.) (Lepidoptera Tortricidae) in Venetian vineyards. Bollettino di Zoologia Agraria e di Bachicultura, serie II, 26(2): 201–230.
  • Marchesini E, Dalla Montà L (1998) I nemici naturali della tignoletta dell’uva nei vigneti del Veneto. Informatore Fitopatologico 1998(9): 3–10.
  • Marchesini E, Dalla Montà L, Sancassani GP (2006) I limitatori naturali delle tignole nell’agroecosistema Vigneto. In: Regione Emilia-Romagna, CRPV: La difesa della vite dalla tignoletta, Bologna 13 novembre 2006: 10–16.
  • Mills NJ, Dixon PL (1993) Increasing parasitism of codling moth in walnuts. Walnut Research Reports 1992: 242–249.
  • Miñarro M, Dapena E (2004) Parasitoids of the codling moth Cydia pomonella in Asturian apple orchards. Boletin de Sanidad Vegetal Plagas 30(3): 507–517.
  • Moreau J, Villemant C, Benrey B, Thiéry D (2010) Species diversity of larval parasitoids of the European grapevine moth (Lobesia botrana, Lepidoptera: Tortricidae): the influence of region and cultivar. Biological control 54(3): 300–306. https://doi.org/10.1016/j.biocontrol.2010.05.019
  • Morley C (1913) The fauna of British India including Ceylon and Burma. Hymenoptera, Vol.3. Ichneumonidae. London, British Museum, 531 pp.
  • Morley C (1915) Ichneumonologia Britannica, V. The Ichneumons of Great Britain. Ophioninae. H. & W. Brown, London (1914), X + 400 pp.
  • Nuzhna AD (2010) Ichneumonidae of the subfamily Anomaloninae (Hymenoptera, Ichneumonidae) in the Crimean fauna. Optimization and Protection of Ecosystems, Simferopol, 22(3): 76–81.
  • Nuzzaci G, Triggiani O (1982) Note sulla biocenosi in Puglia della Lobesia (Polychrosis) botrana (Schiff.) (Lepidoptera: Tortricidae) infeudata a Daphne gnidium L. Entomologica 17: 47–52.
  • Oatman ER (1978) Yponomeutidae, Diamondback Moth (Plutella xylostella (Linnaeus)). In: Bartlett BR, Clausen CP, DeBach P, Goeden R D, Legner EF, McMurtry JA, Oatman ER. Introduced parasites and predators of arthropod pests and weeds: A world review. Agricultural Research Service. United States Department of Agriculture. Agriculture Handbook 480: 240–242.
  • Özsemerci F, Altindisli O, Koclu T, Karsavuran Y (2016) [Natural Parasitization Rate and Larva Parasitoids of Lobesia botrana Denn.-Schiff. (Lepidoptera: Tortricidae) in the Vineyards of Manisa and Izmir Provinces]. Turkey 6th Plant Protection Congress with International Participation, September 5–8, 2016 Konya, Turkey, p 132.
  • Paillot A (1924) La Lyda du pêcher. Étude biologique – Methodes de destruction. Annales Épiphyties 10: 147–237.
  • Petcu I (1978) Specii de Ichneumonidae (Hym.) obţinute prin culturi din diferite insecte dăunătoare II. Analele Ştiinţifice ale Universităţii “Al. I. Cuza” din Iaşi (Serie nouă), Biologie 24: 79–80.
  • Piekarska-Boniecka H (1994) [Contribution to the knowledge of the leaf-rollers (Lepidoptera, Tortricidae) and their parasitoids (Hymenoptera, Ichneumonidae) occurring on the red currant in the environs of Poznan.] (in Polish with English summary). Wiadomosci Entomologiczne 13(3): 185–190.
  • Pinna M, Gremo F, Scaramozzino PL (1989) A preliminary investigation into the influence of biotic and abiotic environmental factors on the winter populations of Lobesia botrana (Den. & Schiff.) in veniyards in Piedmont, Italy (LepidopteraTortricidae). In: Cavalloro R (Ed.) Influence of environmental factors on the control of grape pests, diseases and weeds. Proceedings of a meeting of the EC Experts’ Group, Thessaloniki 6–8 October 1987, 77–86.
  • Pisicá C, Páişescu-Bărbuceanu D (2002) Hymenoptere parazitoide (Fam. Ichneumonidae) la moliile strugurilor. Muzeul Judeţean Argeş, Argessis. [Hymenoptera parasitoids (Ichneumonidae) of the grape moth. Museum Argeş, Argessis]. Studii şi comunicári, seria Stiinţele Naturii 9–10: 207–211.
  • Quicke DLJ (2015) The Braconid and Ichneumonid parasitoid wasps: biology, systematics, evolution and ecology. Wiley-Blackwell, 704 pp.
  • Roat C, Forti D (1994) Indagine sulla parasitizzazione della tignoletta della vite (Lobesia botrana Den. & Schiff.) in Trentino. Bollettino ISMA 1/1994: 37–41.
  • Roman A (1932) The Linnean types of ichneumon flies. Entomologisk Tidskrift 53: 1–16.
  • Ruschka F, Fulmek L (1915) Verzeichnis der an der K. k. Pflanzenschutz-Station in Wien erzogenen parasitischen Hymenopteren. Mitteilungen der K. k. Pflanzenschutzstation, Wien 11, Trunnerstr.1: 390–412.
  • Russ K, Faber B (1978) Studies on the rearing of Trichomma enecator (Ichneumonidae), a parasite of codling moth. Mitteilungen aus der Biologischen Bundesanstalt für Land- und Forstwirtschaft, Berlin-Dahlem: 91–92.
  • Sanborne M (1984) A revision of the world species of Sinophorus Förster (Ichneumonidae). Memoirs of the American Entomological Institute 38: 1–403.
  • Scaramozzino PL, Loni A, Lucchi A (2017a) A review of insect parasitoids associated with Lobesia botrana (Denis & Schiffermüller, 1775) in Italy. 1. Diptera Tachinidae and Hymenoptera Braconidae (Lepidoptera, Tortricidae). ZooKeys 647: 67–100. https://doi.org/10.3897/zookeys.647.11098
  • Scaramozzino PL, Loni A, Lucchi A, Gandini L (2017b) Who’s who in the nests molded by Lobesia botrana on Daphne gnidium? IOBC/WPRS Bulletin 128: 130–134.
  • Schmiedeknecht O (1909) Opuscula Ichneumonologica. IV Band (Fasc. XXI–XXIII). Ophioninae. Blankenburg in Thüringen, 1601–1840.
  • Schnee H (2008) Die Anomaloninae der Sammlung Arnold Förster – Typenrevision und faunistische Anmerkungen (Hymenoptera, Ichneumonidae). Beiträge zur Entomologie 58(2): 249–266.
  • Schwangart F (1913) Die Bekämpfung der Rebschädlinge und die Biologie. Sonder-Abdruck aus den Mitteilungen des Deutschen Weinbau-Vereins: 1–16.
  • Schwangart F (1918) Über Rebenschädlinge und nützlinge. V. Die Schlupfwespen des Traubenwicklers. Zuchtergebnisse. Centralballt für Bakteriologie, Parasitenkunde und Infektionskrankheiten, II Abt., 48(24/25): 543–558.
  • Sciarra G (1915) Contribuzione alla conoscenza della Carpocapsa pomonella (L.). Bollettino del Laboratorio di Zoologia Generale e Agraria della R. Scuola d’Agricoltura in Portici 10: 32–50.
  • Sedivy J (2001) Contribution to the taxonomy and knowledge of hosts of ichneumonids (Hymenoptera: Ichneumonidae). Klapalekiana 37(1–2): 59–69.
  • Shaw MR (2017) A few recommendations on recording host information for reared parasitoids. Hamuli 8(1): 7–9.
  • Shaw MR, Horstmann K (1997) An analysis of host range in the Diadegma nanus group of parasitoids in Western Europe, with a key to species (Hymenoptera: Ichneumonidae: Campopleginae). Journal of Hymenoptera Research 6(2): 273–296.
  • Shaw MR, Horstmann K, Whiffin AL (2016) Two hundred and twenty-five species of reared western Palaearctic Campopleginae (Hymenoptera: Ichneumonidae) in the National Museums of Scotland, with descriptions of new species of Campoplex and Diadegma, and records of fifty-five species new to Britain. Entomologist’s Gazette 66: 245–247.
  • Shaw MR, Stefanescu C, Nouhuys van S (2009) Parasitoids of European butterflies. In: Settele J, Shreeve T, Konvicka M, Van Dyck H (Eds) Ecology of butterflies in Europe. Cambridge University Press, 130–156.
  • Silvestri F (1912) Contribuzioni alla conoscenza degli insetti dannosi e dei loro simbionti. III. La Tignoletta dell’uva (Polychrosis botrana Schiff.) con un cenno sulla Tignola dell’uva (Conchylis ambiguella Hb.). Bollettino del Laboratorio di Zoologia Generale e Agraria, Portici, 6: 246–307.
  • Silvestri F (1923) Contribuzioni alla conoscenza dei Tortricidi delle Querce (I –II). Bollettino del Laboratorio di Zoologia Generale e Agraria della R. Scuola d’Agricoltura in Portici 17: 41–107.
  • Starke H (1956) Ichneumonidenfauna der sächsischen Oberlausitz. Natura Lusatica (Bautzen) 3: 17–92.
  • Stellwaag F (1921) Die Schmarotzerwespen als Parasiten. Monographie der deutschen Gesellschaft für angewandte Entomologie 6 (Supplement 2 to Volume VII), 98 pp.
  • Stellwaag F (1928) Die Weinbauinsekten der Kulturländer, Lehr- und Handbuch. Verlagsbuchhandlung Paul Parey, Berlin, 884 pp.
  • Syme PD (1971) Rhyacionia buoliana (Schiff.) European pine shoot moth (Lepidoptera: Olethreutidae). Biological Control Programmes against Insects and Weeds in Canada 1959–1968, Commonwealth Agricultural Bureaux, 1971 Technical Communication 4: 194–205.
  • Syme PD (1984) Rhyacionia buoliana (Schiff.), European pine shoot moth (Lepidoptera: Tortricidae). In: Kelleher JS, Hulme MA (editors) Biological Control Programmes against Insects and Weeds in Canada 1969–1980. Commonwealth Agricultural Bureaux, London, 387–394.
  • Telenga NA (1934) Parasiten und ihre Bedeutung in der Dynamik des Traubenwicklers (Polychrosis botrana Schiff.). Journal of Pest Science 10(9): 101–106. https://doi.org/10.1007/BF02336199
  • Thiéry D (2008) Les tordeuses nuisibles à la vigne. In: Esmenjaud D, Kreiter S, Martinez M, Sforza R, Thiéry D, van Helden M, Yvan M (Eds) Ravageurs de la vigne. Deuxième édition, Féret, Bordeaux, 214–246.
  • Thiéry D, Xuereb A, Villemant C, Sentenac G, Delbac L, Kuntzman P (2001) Les parasites de tordeuses de vignobles: apercu de quelques especes presentes dans 3 regions viticoles françaises. IOBC/WPRS Bulletin 24(7): 135–141.
  • Thompson WR (1946) A catalogue of the parasites and predators of insect pest. Section 1 Parasite Host Catalogue, Part 8. Parasites of the Lepidoptera (N-P). Commonwealth Agricultural Bureaux, Farnham Royal, UK., Reprinted 1960 with Errata, 523 pp.
  • Thompson WR (1957) A catalogue of the parasites and predators of insect pests. Section 2. Host parasite catalogue, Part 4. Hosts of the Hymenoptera (Ichneumonidae). Commonwealth Agricultural Bureaux, Commonwealth Institute of Biological Control, Ottawa, 333–561.
  • Thompson WR (1958) A catalogue of the parasites and predators of insect pests. Section 2. Host parasite catalogue, Part 5. Hosts of the Hymenoptera (Miscogasteridae to Trigonalidae), Lepidoptera ans Strepsittera. Commonwealth Agricultural Bureaux, Commonwealth Institute of Biological Control, Ottawa, Ontario, Canada, 562–698.
  • Thompson WR, Parker HL (1928) The European corn borer and its controlling factors in Europe. U.S. Dept. of Agriculture Technical Bulletin 59: 1–62.
  • Thompson WR, Parker HL (1930) The morphology and biology of Eulimneria crassifemur, an important parasite of the European corn borer. Journal of Agricultural Research 40(4): 321–345.
  • Thomson CG (1887) XXXV. Försök till uppställning och beskrifning af aterna inom slägtet Campoplex (Grav.). Opuscula Entomologica (Lund) 11: 1043–1182.
  • Thomson CG (1892) XLV. Bidrag till kännedomen om slägtet Anomalon (Grav). Opuscula Entomologica, Lund, 16: 1752–1772.
  • Townes HK (1971) The genera of Ichneumonidae, part 4. Memoirs of the American Entomological Institute 17: 1–372.
  • Townes HK, Momoi S, Townes M (1965) A catalogue and reclassification of the eastern Palearctic Ichneumonidae. Memoirs of the American Entomological Institute 5: 1–661.
  • Unruh T, Short R, Herard F, Chen K, Hopper K, Pemberton R, Lee JH, Ertle L, Swan K, Fuester R, Lagasa E (2003) Introduction and establishment of parasitoids for the biological control of the apple ermine moth, Yponomeuta malinellus (Lepidoptera: Yponomeutidae), in the Pacific Northwest. Biological Control 28(3): 332–345. https://doi.org/10.1016/S1049-9644(03)00101-4
  • Vas Z, Mifsud D, Broad GR (2015) New records of ichneumon wasps (Hymenoptera, Ichneumonidae) from Malta. Bullettin of the Entomological Society of Malta 7: 139–142.
  • Villemant C, Delvare G, Martinez M, Sentenac G, Kuntzmann P (2011) Parasitoïdes de tordeuses. In: Sentenac G (Ed.) La faune auxiliaire des vignobles de France. Editions France Agricole, Paris, 119–140.
  • Voukassovitch P (1924) Contribution à l’étude de l’eudemis (Polychrosis botrana, Schiff.), de la pyrale de la vigne (Oenophthira pilleriana Schiff.) et de leurs parasites. E.H. Guitard, Toulouse, 248 pp.
  • Westwood JO (1840) Synopsis of the genera of British insects. An introduction to the modern classification of insects, founded on the natural habits and corresponding organisation of the different families. Part 2, London, 11, 587 + 158 pp.
  • Wildbolz T, Staub A (1985) Der Schlüpfverlauf männlicher und weiblicher Apfelwicklerfalter (Cydia pomonella) und der Raupenparasiten im Insektarium. Mitteilungen der Schweizerischen Entomologischen Gesellschaft 58: 199–204.
  • Yu DSK, Achterberg C van, Horstmann K (2012) Taxapad 2012, Ichneumonoidea 2011. Database on flash-drive. Ottawa. Available from: Yu DSK (1997–2012) Home of Ichneumonoidea. http://www.taxapad.com [accessed: January 13, 2018]
  • Yu DSK, Horstmann K (1997) A Catalogue of the World Ichneumonidae (Hymenoptera). Memoirs of the American Entomological Institute 58, parts 1+2, 1558 pp.
  • Zaemdzhikova GI (2017) Ichneumon wasps (Hymenoptera: Ichneumonidae) reared from tortrix moths (Lepidoptera: Tortricidae) in oak forests in Sofia region, Bulgaria. Acta Zoologica Bulgarica 8: 123–129.
  • Zangheri S, Dalla Montà L, Duso C (1987) Observations on biology and control of grape moths in Venetia. Proceedings of a meeting of the EC Experts' Group, Portoferraio, 26–28 September 1985. Balkema, Rotterdam, 27–37.
  • Zapryanov A (1985) [The parasites of the family Ichneumonidae in Bulgaria and their hosts in the various agrocenoses. ] (in Russian with English summary) Pochvoznanie Agrokhimiya i Rastitelna Zashtita 20(4): 135–145.
  • Zapryanov A, Stoeva R (1982) [The parasitic entomofauna of Lobesia botrana Schiff. (Lepidoptera, Tortricidae) in south-western Bulgaria and its role in reducing the density of the pest]. (in Russian) Gradinarska-i-Lozarska-Nauka 19(3): 74–80.
  • Zocchi R (1952) Contributi alla conoscenza degli insetti delle piante forestali. II. Note biologiche sull’Evetria buoliana Schiff. (Lepidoptera: Tortricidae). Redia 37: 346–369.
  • Zwakhals K, Achterberg C van (2017) Fauna Europaea: Ichneumonidae. Fauna Europaea vers.2017.06 http://fauna-eu.org