Glyptapanteles indiensis (Marsh, 1979)

Hoecherl, Amelie, Shaw, Mark R., Boudreault, Caroline, Rabl, Dominik, Haszprunar, Gerhard, Raupach, Michael J., Schmidt, Stefan, Baranov, Viktor & Fernandez-Triana, Jose, 2024, Scratching the tip of the iceberg: integrative taxonomy reveals 30 new species records of Microgastrinae (Braconidae) parasitoid wasps for Germany, including new Holarctic distributions, ZooKeys 1188, pp. 305-386 : 305

Glyptapanteles indiensis (Marsh, 1979)

Material examined.

Czech Republic: South Moravia: Obora Soutok, Lanžhot, 48.69, 16.945, 165 m, 14.v.2013, leg. P. Drozd, BC- ZSM-HYM-23872-A04; ex.? Alsophila auscularia , 05.v.2015, leg. M. Sigut, BC- ZSM-HYM-27569-F09; ex. Operophtera brumata , 08.v.2015, leg. P. Drozd, BC- ZSM-HYM-23872-F08 ; Germany: Baden-Württemberg: Malsch, Hansjakobstr. 7, Urban Garden , 48.884, 8.32, 120 m, Malaise trap, 11.x.2020, leg. D. Doczkal, ZSM-HYM-33154-B09 ; Bavaria: Markt Nordheim, Kehrenberg, 49.547, 10.366, 419 m, canopy fogging, 10.vii.2020, leg. B. Leroy, ZSM-HYM-42393-B07; Rhön Fladungen, NSG Schwarzes Moor, Kermi-Hochmoor, 50.512, 10.069, 780 m, Malaise trap, 23.viii.2017, leg. D. Doczkal, ZSM-HYM-33165-A08; Rhön Hausen, Eisgraben, basalt block heap at forest edge, 50.503, 10.09, 735 m, Malaise trap, 23.vii.2018, leg. D. Doczkal, ZSM-HYM-33166-C03; 9.viii.2018, leg. D. Doczkal, ZSM-HYM-33166-D10; Südpark, 48.103, 11.509, 550 m, ex. Operophtera brumata , 28.v.2021, leg. W. Langer, ZSM-HYM-ZLAB01-F05 ; India: Kashmir Sprinagar , ex. Lymantria obfuscata , [collector unknown], 2.v.1977, CNCHYM 03231; CNCHYM 03232 ; Japan: Aichi: Mt. Chausu , 35.2275 137.655558, 1300 m, 9.vii.1995, leg. K. Yamagishi, JMIC 0011 .

Geographical distribution.

NEA, OTL, PAL.

NEA: USA (PA), OTL: India, PAL: Czech Republic*, Germany*, Japan*.

Molecular data.

BOLD:ABY2372.

Host information.

Erebidae : type reared from Lymantria obfuscata (Marsh, 1979); also Lymantria dispar (Linnaeus, 1758); Geometridae *: Operophtera brumata * (Linnaeus, 1758).

Notes.

We record G. indiensis for the first time in the Palaearctic region, based on specimens from Germany, Japan and Czech Republic. This species is morphologically similar, especially in habitus, to several Glyptapanteles species. Our identification was therefore based on a careful study (detailed below) which included a combination of morphology (see Figs 25 , 26 , both examination of authenticated specimens and consulting original descriptions and other relevant papers (e.g., Muesebeck 1928; Nixon 1973; Marsh 1979; Papp 1983)), DNA barcodes (available for all species discussed below, see Suppl. materials and Fig. 24 ) and hosts (available for most species mentioned above, except for G. popovi ). The German, Japanese (JMIC 0011) and Czech specimens (BC- ZSM-HYM-23872-A04, BC- ZSM-HYM-23872-F08, BC- ZSM-HYM-27569-F09) were identified by morphological comparison with two paratypes of G. indiensis deposited in the CNC as well as information from the original description ( Marsh 1979). One of those paratypes (a male specimen (CNCHYM 03232) reared from Lymantria obfuscata in India, apparently part of the same brood as the female paratype deposited at the CNC (CNCHYM 03231)) was successfully barcoded and the 455 bp sequence matches the remaining sequences in this BIN by 99.5%. Glyptapanteles indiensis is known to parasitise Lymantria obfuscata in India and Lymantria dispar (at least in the laboratory), and therefore is of interest as a biocontrol agent ( Marsh 1979), although we are not aware of published data confirming the parasitisation of L. dispar by G. indiensis in the wild. However, we have additional data from a metabarcoding study in Germany including caterpillars that were collected as part of a canopy fogging project. There, seven individual caterpillars of L. dispar had more than 30 reads of sequences that match the barcoding cluster that we associated with G. indiensis (99.6-100% bp similarity), therefore providing at least an indirect confirmation of the parasitisation of L. dispar in the wild by this wasp species. Additionally, we examined two specimens (ZSM-HYM-ZLAB01-F05 and BC- ZSM-HYM-23872-F08) which were reared from the Geometridae Operophtera brumata and represent a new host family record for this species. The aforementioned metabarcoding data suggests that there might be additional hosts for this species; however, this would need to be confirmed by rearing.

Other species of Glyptapanteles parasitising Lymantria dispar are Glyptapanteles liparidis (BOLD:AAV2164, including several reared specimens from this host such as WAM 0445=MRS_JFT 0028, BC- ZSM-HYM-23872-A02, BC- ZSM-HYM-23872-A05) and Glyptapanteles porthetriae (BOLD:ACL7229, including a reared specimen from this host: BC- ZSM-HYM-23872-F09). The many available barcodes from both G. porthetriae and G. liparidis are very distinct and clearly separated from those of G. indiensis (> 3.5% K2P-distance, see Fig. 24 ), and there are also morphological differences between these three species as detailed in Marsh (1979).

The known hosts of G. mygdonia include Operophtera brumata and the multiple hosts recorded for G. vitripennis in the literature (many of them likely incorrect) include both O. brumata and L. dispar . The many available sequences of G. mygdonia (BOLD:AAU5027) and G. vitripennis (BOLD:AAA7148) are also very distinctive and far apart from those of Glyptapanteles indiensis [The sequences of G. vitripennis and G. liparidis are relatively very close (2.13% p-distance); furthermore, G. vitripennis seems to include a complex of species that remains unresolved, but that is beyond the scope of the present paper]. There are also morphological differences between these species and G. indiensis ( Nixon 1973). Two characters we found were useful are the relative length of the ovipositor sheaths, which is much longer in G. indiensis as compared to the other two species and the lack of a curved spine on the fore tarsus for G. indiensis (present in both G. mygdonia and G. vitripennis ).

The last species we compared to G. indiensis was G. popovi , which is much less understood. Until now, G. popovi was only known from Turkey and Turkmenistan ( Fernandez-Triana et al. 2020) and there is no host known for this species. Based on information from Telenga (1955), Tobias (1986), and the study of a specimen of G. popovi from Armenia (CNCHYM 01335) identified by Kotenko in 1981 and deposited in the CNC these two species are different. Analyses of available DNA sequences strongly support that (these two species are clearly apart by more than 5% K2P-distance, compare Fig. 25 ). We found German specimens from both species and thus both species are recorded from Germany in this paper (see also comments below, under G. popovi ). Glyptapanteles indiensis is illustrated in Figs 25 , 26 .

Figures

Figure 24. Neighbour-joining topology of the COI barcoding region of Glyptapanteles indiensis, G. popovi and morphologically similar species, based on Kimura 2 - parameter distances. Numbers next to nodes represent non-parametric bootstrap values> 90 % (1,000 replicates). The aligned sequences and N-J topology can be reviewed in Suppl. materials 6, 7.

Figure 25. Glyptapanteles indiensis (Marsh, 1979), female (ZSM-HYM- 33154 - B 09) A lateral and B dorsal views. Length of the specimen: 3.5 mm.

Figure 26. Glyptapanteles indiensis (Marsh, 1979), female paratype (CNCHYM 03231) A lateral view B forewing C head frontal view D mesosoma E metasoma.