A morphological, biological and molecular approach reveals four cryptic species of Trissolcus Ashmead (Hymenoptera, Scelionidae), egg parasitoids of Pentatomidae (Hemiptera) Author Tortorici, Francesco https://orcid.org/0000-0002-0071-3292 Dipartimento di Scienze Agrarie, Forestali e Alimentari (DISAFA), Entomologia Generale e Applicata, University of Torino, Largo P. Braccini 2, 10095 Grugliasco (TO), Italy Author Talamas, Elijah J. https://orcid.org/0000-0002-1048-6345 Florida Department of Agriculture and Consumer Service, Division of Plant Industry, Gainesville, Florida, USA billy.jenkins@GMAIL.COM Author Moraglio, Silvia T. https://orcid.org/0000-0001-9922-5071 Dipartimento di Scienze Agrarie, Forestali e Alimentari (DISAFA), Entomologia Generale e Applicata, University of Torino, Largo P. Braccini 2, 10095 Grugliasco (TO), Italy Author Pansa, Marco G. Dipartimento di Scienze Agrarie, Forestali e Alimentari (DISAFA), Entomologia Generale e Applicata, University of Torino, Largo P. Braccini 2, 10095 Grugliasco (TO), Italy Author Asadi-Farfar, Maryam https://orcid.org/0000-0003-4921-351X Department of Plant Protection, Faculty of Agriculture, Urmia University, Urmia, Iran Author Tavella, Luciana Dipartimento di Scienze Agrarie, Forestali e Alimentari (DISAFA), Entomologia Generale e Applicata, University of Torino, Largo P. Braccini 2, 10095 Grugliasco (TO), Italy Author Caleca, Virgilio Department of Agricultural, Food and Forest Sciences, University of Palermo, Edificio 5, Viale delle Scienze, 90128 Palermo, Italy text Journal of Hymenoptera Research 2019 2019-11-18 73 153 200 http://dx.doi.org/10.3897/jhr.73.39052 journal article http://dx.doi.org/10.3897/jhr.73.39052 1314-2607-73-153 93B22F06E829401CB2E31C08169706FB 76BE7E90630A510F9FF3A1174BBB41FC 3553345 Trissolcus belenus (Walker) Figures 4 , 8 , 12 , 16 , 20 , 21 , 26 , 30 , 33 , 37 , 41 , 45-48 , 49-51. Telenomus Belenus Walker, 1836: 352 (original description). Telenomus arminon Walker, 1838: 457 (original description). Telenomus Nigrita Thomson, 1860: 172 (original description, synonymized by Kozlov (1968) ); Kozlov 1968 : 214 (junior synonym of Trissolcus grandis (Thomson)). Telenomus frontalis Thomson, 1860: 170 (original description, synonymized by Kozlov (1968) ); Kozlov 1968 : 214 (junior synonym of Trissolcus grandis (Thomson)). Telenomus grandis Thomson, 1860: 169 (original description). Telenomus nigripes Thomson, 1860: 170 (original description, synonymized by Kozlov (1968) ); Kozlov 1968 : 214 (junior synonym of Trissolcus grandis (Thomson)); Fergusson 1984 : 230 (lectotype designation); Johnson 1992 : 629 (type information). Telenomus ovulorum Thomson, 1860: 171 (original description, synonymized by Mayr (1879) ); Mayr 1879 : 704 (junior synonym of Telenomus semistriatus (Nees von Esenbeck)). Teleas (?) Pentatomae Rondani: Rondani 1874 : 135 (nomen nudum). Teleas pentatomae Rondani, 1877: 199 (original description). Telenomus ovulorum Thomson: Mayr 1879 : 704. Junior synonym of Telenomus semistriatus (Nees von Esenbeck) Telenomus nigritus Thomson: Dalla Torre 1898 : 517 (emendation). Telenomus pentatomae (Rondani): Dalla Torre, 1898: 518 (generic transfer). Allophanurus Arminon (Walker): Kieffer 1912 : 12 (description, generic transfer). Aphanurus Belenus (Walker): Kieffer 1912 : 83 (description, generic transfer). Aphanurus Frontalis (Thomson): Kieffer 1912 : 81 (description, generic transfer). Aphanurus Grandis (Thomson): Kieffer 1912 : 76 (description, generic transfer). Aphanurus Nigrita (Thomson): Kieffer 1912 : 79 (description, generic transfer). Aphanurus nigripes (Thomson): Kieffer 1912 : 75 (description, generic transfer). Liophanurus Pentatomae (Rondani): Kieffer 1912 : 69 (description, generic transfer). Allophanurus arminon (Walker): Kieffer 1926 : 23 (description, keyed). Liophanurus pentatomae (Rondani): Kieffer 1926 : 71 (description). Microphanurus belenus (Walker): Kieffer 1926 : 91, 102 (description, generic transfer, keyed). Microphanurus frontalis (Thomson): Kieffer 1926 : 91, 103 (description, generic transfer, keyed). Microphanurus grandis (Thomson): Kieffer 1926 : 91, 99 (description, generic transfer, keyed); Debauche 1947 : 256 (description). Microphanurus nigripes (Thomson): Kieffer 1926 : 91, 98 (description, generic transfer, keyed). Microphanurus nigritus (Thomson): Kieffer 1926 : 91, 100 (description, generic transfer, keyed). Asolcus grandis (Thomson): Masner 1959 : 376. (diagnosis, variation); Delucchi 1961 : 44, 60 (description, keyed); Voegele 1964 : 28 (keyed); Javahery 1968 : 419 (keyed); Voegele 1969 : 150 (keyed). Trissolcus grandis (Thomson) syn. nov.: Viktorov 1967 : 91 (generic transfer, keyed); Safavi 1968 : 416 (keyed); Kozlov 1968 : 200, 214 (description, lectotype designation, synonymy, keyed); Fabritius 1972 : 32, 35. (keyed; host catalogue; distribution); Viggiani and Mineo 1974 : 156, 160, 161 (description, keyed); Kozlov and Le 1977 : 512 (synonymy, keyed); Kozlov 1978 : 636 (description); Kozlov 1981 : 187 (keyed); Kozlov and Kononova 1983 : 110 (description); Johnson 1992 : 629 (cataloged, type information); Kononova 1995 : 96 (keyed); Doganlar 2001 : 112 (description); Kocak and Kilincer 2003 : 302, 307 (keyed, description); Fabritius and Popovici 2007 : 158 (host informations, distribution); Buhl & O'Connor , 2010: 154 (distribution); Ali 2011 : 10 (keyed); Ghahari et al. 2011 : 596 (host association, listed); Guz et al. 2013 : 87 (description, phylogenetic relationships); Petrov 2013 : 326 (keyed); Kononova 2014 : 1424 (keyed); Kononova 2015 : 262 (keyed); Talamas et al. 2017 : 129, 135 (junior synonym of Trissolcus semistriatus (Nees von Esenbeck), type information). Asolcus nixomartini Javahery, 1968: 419, 429 (original description, keyed, synonymized by Kozlov and Le (1977) ); Kozlov, and Le 1977 : 512 (junior synonym of Trissolcus grandis (Thomson)); Johnson 1992 : 629 (type information). Asolcus silwoodensis Javahery, 1968: 419, 425 (original description, keyed, synonymized by Kozlov and Le (1977) ); Kozlov, and Le 1977 : 512 (junior synonym of Trissolcus grandis (Thomson)); Johnson 1992 : 629 (type information). Trissolcus pentatomae (Rondani) syn. nov.: Bin 1974 : 463 (generic transfer, lectotype designation); Johnson 1992 : 634 (cataloged, type information); Talamas et al. 2017 : 130, 135 (junior synonym of Trissolcus semistriatus (Nees von Esenbeck), type information). Trissolcus belenus (Walker): Fergusson 1978 : 120 (generic transfer); Fergusson 1984 : 230 (lectotype designation); Johnson 1992 : 623 (cataloged, type information); Kononova 2014 : 1426 (possibly in Telenomus ); Kononova 2015 : 264 (possibly in Telenomus ). Trissolcus nigripes (Thomson) syn. nov.: Fergusson 1978 : 120 (generic transfer). Trissolcus nixomartini (Javahery) syn. nov.: Fergusson 1978 : 120 (generic transfer); Fergusson 1984 : 230 (type information). Trissolcus silwoodensis (Javahery) syn. nov.: Fergusson 1978 : 120 (generic transfer); Fergusson 1984 : 230 (type information). Trissolcus arminon (Walker) syn. nov.: Fergusson 1983 : 208 (generic transfer, description, lectotype designation); Fergusson 1984 : 230 (type information); Johnson 1992 : 622 (cataloged, type information). Trissolcus ovulorum (Thomson) comb. nov., syn. nov. Diagnosis. The presence of setae on the first laterotergite ( Figures 30 , 45 ) allows T. belenus to be easily diagnosed, as only two other Palearctic species share this character: T. saakowi and T. mitsukurii (Ashmead). Both of these species have distinct notauli, which are absent in T. belenus ( Figures 20 , 22 ). Additionally, the hyperoccipital carina is entirely absent in T. belenus ( Figures 33 , 47 , 49 ), whereas it is complete in T. saakowi and present posterior to the lateral ocellus in T. mitsukurii . Description. Body length: 1.03-1.1 mm, median = 1.06 mm, SD = 0.02, n = 20. Body color: head, mesosoma, and metasoma black. Head . FCI = 1.4; LCI = 1.9; IOS = 0.3 mm; OOL:POL:LOL = 1:12:5.8. Color of radicle: dark brown. Length of radicle: about equal to width of clypeus. Color of A1-A6 in female: distal A2 yellow to light brown, otherwise black. Color of A7-A11 in female: black. Number of papillary sensilla on A6: 0. Number of papillary sensilla on A7: 2. Facial striae: absent. Number of clypeal setae: 6. Shape of gena in lateral view: narrow. Genal carina: present only at base of mandible. Malar striae: absent. Sculpture of malar sulcus: distinctly and sparsely striate. Orbital furrow: uniform in width between midpoint of eye and malar sulcus. Macrosculpture of frons directly dorsal to the antennal scrobe: coarsely rugose. Preocellar pit: present. Setation of lateral frons: sparse; moderately dense. Punctation of lateral frons: sparse. Sculpture directly ventral to preocellar pit: dorsoventrally fluted. Rugae on lateral frons: weakly developed to absent. OOL: less than one ocellar diameter. Hyperoccipital carina: absent. Macrosculpture of posterior vertex: absent. Microsculpture on posterior vertex along occipital carina: granulate. Anterior margin of occipital carina: crenulate. Medial part of occipital carina in dorsal view: rounded. Mesosoma . Epomial carina: present. Macrosculpture of lateral pronotum directly anterior to netrion: finely rugulose. Netrion sulcus: complete. Pronotal suprahumeral sulcus in posterior half of pronotum: undifferentiated from sculpture of dorsal pronotum. Number of episternal foveae: 2. Course of episternal foveae ventrally: distinctly separate from postacetabular sulcus. Course of episternal foveae dorsally: distinctly separate from mesopleural pit. Subacropleural sulcus: present. Speculum: transversely strigose. Mesopleural pit: extending ventrally into dorsoventral furrow parallel to mesopleural carina. Mesopleural carina: well defined anteriorly, poorly defined to absent posteriorly. Sculpture of femoral depression: smooth. Patch of striae at posteroventral end of femoral depression: present, striae oblique to long axis of femoral depression. Setal patch at posteroventral end of femoral depression: present as a line of setae. Microsculpture of anteroventral mesopleuron: present throughout. Macrosculpture of anteroventral mesopleuron: absent. Postacetabular sulcus: comprised of large cells. Mesopleural epicoxal sulcus: comprised of cells. Setation of posteroventral metapleuron: absent. Sculpture of dorsal metapleural area: absent. Posterodorsal metapleural sulcus: present as a line of foveae. Paracoxal sulcus in ventral half of metapleuron: indistinguishable from sculpture. Length of anteroventral extension of metapleuron: elongate, extending to base of mesocoxa. Apex of anteroventral extension of metapleuron: rounded. Metapleural epicoxal sulcus: present as coarse rugae. Mesoscutal humeral sulcus: comprised of cells. Median mesoscutal carina: absent. Microsculpture of mesoscutum: imbricate-punctate anteriorly, becoming longitudinally imbricate-strigate posteriorly. Mesoscutal suprahumeral sulcus: comprised of cells. Length of mesoscutal suprahumeral sulcus: two-thirds the length of anterolateral edge of mesoscutum. Parapsidal line: absent. Notaulus: absent. Median protuberance on anterior margin of mesoscutellum: absent. Shape of dorsal margin of anterior lobe of axillar crescent: acute. Sculpture of anterior lobe of axillar crescent: dorsoventrally strigose. Area bound by axillar crescent: smooth. Macrosculpture of mesoscutellum: absent. Microsculpture on mesoscutellum: imbricate-punctate laterally to granulate medially. Median mesoscutellar carina: absent. Setation of posterior scutellar sulcus: present. Form of metascutellum: single row of cells. Metanotal trough: foveate, foveae occupying more than half of metanotal height. Metapostnotum: invaginated near lateral edge of metascutellum. Length of postmarginal vein: about twice as long as stigmal vein. Color of legs: coxae dark brown to black, femora and tibia dark brown with yellowish tips, trochanters and tarsi yellow to pale brown. Anteroventral area of hind femora: not covered by setae. Anteromedial portion of metasomal depression: smooth. Metasoma . Width of metasoma: about equal to width of mesosoma. Longitudinal striae on T1 posterior to basal costae: pair of longitudinal submedial carinae separate a lateral smooth area from an internal area where striate sculpture starts with basal grooves. Number of sublateral setae (on one side): 1. Setation of laterotergite 1: present. Length of striation on T2: extending two-thirds the length of the tergite. Setation of T2: present in a transverse line and along lateral margin. Setation of laterotergite 2: present. Host associations . Pentatomidae : Aelia rostrata ; Arma custos ; Carpocoris sp.; Dolycoris sp.; Graphosoma italicum Mueller ; Palomena prasina ; Picromerus bidens (L.); Piezodorus sp.; sentinel frozen eggs of Halyomorpha halys . Scutelleridae : Eurygaster integriceps Puton; Eurygaster maura . Link to distribution map. [https://hol.osu.edu/map-large.html?id=3190] Material examined. Lectotype , male Telenomus Belenus : England and Western Europe : no date, NMINH_2018_11_49 (deposited in NMID) ; Lectotype , female, Telenomus arminon : United Kingdom : England, Dorset County , Lyme Regis , no date, NMINH_2018_11_46 (deposited in NMID) ; Holotype , female, Asolcus nixomartini : United Kingdom : England, Windsor and Maidenhead Unit. Auth., Silwood Park, 1966, reared from egg, M. Javahery , B.M. TYPE HYM. 9.798 (deposited in BMNH) ; Paratypes of Asolcus nixomartini : United Kingdom : 1 female , 2 males , UNIPA-HYM-S01317- S01318 (BMNH); OSUC 17734 (BMNH) ; Holotype , female, Asolcus silwoodensis : United Kingdom : England, Windsor and Maidenhead Unit. Auth., Silwood Park, 1966, reared from egg, M. Javahery , B.M. TYPE HYM. 9.797 (deposited in BMNH) ; Paratypes of Asolcus silwoodensis : United Kingdom : 4 females , 4 males , UNIPA-HYM-S01309- S01316 (BMNH) . Syntype males, Telenomus ovulorum Thomson : Sweden : no date, Boheman , NHRS-HEVA 000006872 (deposited in NHRS) . Lectotype , female, Telenomus nigripes : Sweden : Vaestra Goetaland , no date, Boheman , NHRS-HEVA 000006873 (deposited in NHRS) . Paratype of T. nixomartini : United Kingdom : 1 male , OSUC 17734 (BMNH) . Other material : ( 437 females , 67 males , 21 pins with multiple specimens). China : 1 female , OSUC 571231 (OSUC) . Iran : 16 females , HMIM-HYM-05-06, 08-09, 011-012, 014, 027, 039 (HMIM); USNMENT01223080-01223082, 01223425, 01223430, 01223435, 01223440 (UNIPA) . Italy : 366 females , 63 males , 17 pins with multiple specimens, DISAFA-draw1465-HYM-0006-0219 (DISAFA); MSNG -HYM-0001-0004, USNMENT01223249-01223258 (MCSN); USNMENT01223090-01223130, 01223132-01223139, 01223230-01223246 (UNIPA) . Morocco : 24 female , 1 pin with multiple specimens, OSUC 17729 (BMNH); USNMENT01223131 (UNIPA) . Portugal : 6 females , 1 male , 1 pin with multiple specimens, USNMENT00916191, 00916210-00916213, 00916217 (BMNH) . Russia : 4 females , 2 males , 2 pins with multiple specimens, OSUC 17796-17797 (BMNH) . Sweden : 12 females , 2 males , UNIPA-HYM-S01306- S01307 , USNMENT00916047, USNMENT00916051, USNMENT00916052, USNMENT00916070, USNMENT00916302-00916309 (BMNH) . Switzerland : 6 females , DISAFA-draw1465-HYM-0001-0005 (DISAFA); USNMENT01109059 (USNM) . Tanzania : 1 female , USNMENT01223480 (MZUF) . United Kingdom : 1 female , 1 male , UNIPA-HYM-S01308 (BMNH); USNMENT00896318 (CNCI) .