Integrative taxonomy and analysis of species richness patterns of nocturnal Darwin wasps of the genus Enicospilus Stephens (Hymenoptera, Ichneumonidae, Ophioninae) in Japan

Abstract

The predominantly tropical ophionine genus Enicospilus Stephens, 1835 is one of the largest genera of Darwin wasps (Hymenoptera, Ichneumonidae), with more than 700 extant species worldwide that are usually crepuscular or nocturnal and are parasitoids of Lepidoptera larvae. In the present study, the Japanese species of Enicospilus are revised using an integrative approach (combined morphology and DNA barcoding). On the basis of 3,110 specimens, 47 Enicospilus species are recognised in Japan, eight of which are new species (E. acutus Shimizu, sp. nov., E. kunigamiensis Shimizu, sp. nov., E. limnophilus Shimizu, sp. nov., E. matsumurai Shimizu, sp. nov., E. pseudopuncticulatus Shimizu, sp. nov., E. sharkeyi Shimizu, sp. nov., E. takakuwai Shimizu, sp. nov., and E. unctus Shimizu, sp. nov.), seven are new records from Japan (E. jilinensis Tang, 1990, E. laqueatus (Enderlein, 1921), E. multidens Chiu, 1954, stat. rev., E. puncticulatus Tang, 1990, E. stenophleps Cushman, 1937, E. vestigator (Smith, 1858), and E. zeugos Chiu, 1954, stat. rev.), 32 had already been recorded in Japan; three (E. biharensis Townes, Townes & Gupta, 1961, E. flavicaput (Morley, 1912), and E. merdarius (Gravenhorst, 1829)) have been erroneously recorded from Japan based on misidentifications, and four names that were previously on the Japanese list are deleted through synonymy. The following taxonomic changes are proposed: E. vacuus Gauld & Mitchell, 1981, syn. nov. (= E. formosensis (Uchida, 1928)); E. multidensstat. rev.; E. striatus Cameron, 1899, syn. nov. = E. lineolatus (Roman, 1913), syn. nov. = E. uniformis Chiu, 1954, syn. nov. = E. flatus Chiu, 1954, syn. nov. = E. gussakovskii Viktorov, 1957, syn. nov. = E. striolatus Townes, Townes & Gupta, 1961, syn. nov. = E. unicornis Rao & Nikam, 1969, syn. nov. = E. unicornis Rao & Nikam, 1970, syn. nov. (= E. pungens (Smith, 1874)); E. iracundus Chiu, 1954, syn. nov. (= E. sakaguchii (Matsumura & Uchida, 1926)); E. sigmatoides Chiu, 1954, syn. nov. (= E. shikokuensis (Uchida, 1928)); E. yamanakai (Uchida, 1930), syn. nov. (= E. shinkanus (Uchida, 1928)); E. ranunculus Chiu, 1954, syn. nov. (= E. yezoensis (Uchida, 1928)); and E. zeugosstat. rev. = E. henrytownesi Chao & Tang, 1991, syn. nov. In addition, the following new regional and country records are also provided: E. flavocephalus (Kirby, 1900), E. puncticulatus, and E. vestigator from the Eastern Palaearctic region, E. laqueatus from the Eastern Palaearctic and Oceanic regions, and E. maruyamanus (Uchida, 1928) from the Oriental region; E. abdominalis (Szépligeti, 1906) from Nepal, E. flavocephalus from Laos, E. formosensis from Laos and Malaysia, E. insinuator (Smith, 1860) from Taiwan, E. maruyamanus from India and Philippines, E. nigronotatus Cameron, 1903, E. riukiuensis (Matsumura & Uchida, 1926), and E. sakaguchii from Indonesia, E. pungens from 14 countries (Australia, Bhutan, Brunei, Indonesia, Laos, Malaysia, Nepal, New Caledonia, Papua New Guinea, Philippines, Solomon Islands, Sri Lanka, Tajikistan, and Taiwan), and E. yezoensis from South Korea. An identification key to all Japanese species of Enicospilus is proposed. Although 47 species are recognised in the present study, approximately 55 species could potentially be found in Japan based on ACE and Chao 1 estimators. The latitudinal diversity gradient of Enicospilus species richness is also tested in the Japanese archipelago based on the constructed robust taxonomic framework and extensive samples. Enicospilus species richness significantly increases towards the south, contrary to the ‘anomalous’ pattern of some other ichneumonid subfamilies.

Uncovering the Brazilian Orthocentrinae (Hymenoptera: Ichneumonidae) fauna: high diversity at high elevation

“…The elevational distribution most commonly found for ichneumonids is a mid-elevation peak in species richness (van Noort 2004;Peck et al 2008;Veijalainen et al 2014b). In apparent disagreement with this general trend for elevational gradients, latitudinal trends of higher diversity in the tropics, even in the lowlands, seem to be consistently corroborated by recent publications (Veijalainen et al 2012(Veijalainen et al , 2013Timms et al 2015;Shimizu et al 2020), indicating that the anomalous pattern therewith observed and theorised for ichneumonids (Owen and Owen 1974;Askew and Shaw 1986;Gauld 1986Gauld , 1987 might be caused by biased data, especially for smallbodied koinobiont species that are harder to identify (Sääksjärvi et al 2004;Santos and Quicke 2011;Quicke 2012), such as the Orthocentrinae.…”

“…Such studies are instrumental to unravelling the diversity of ichneumonids in the Neotropics, and they corroborate the perception that theories regarding latitudinal patterns of distribution (e.g., Owen and Owen 1974;Janzen 1981;Askew and Shaw 1986;Gauld 1986Gauld , 1987 depend on substantial accumulation of information from tropical regions to be relevant (Quicke 2012). In fact, recent studies on latitudinal patterns repeatedly show higher diversity in the tropics for most ichneumonids (Veijalainen et al 2012(Veijalainen et al , 2013Timms et al 2015;Shimizu et al 2020). Local intensive faunistic assessments of the Ichneumonoidea along elevational gradients have been helpful in understanding diversity patterns in this group, which most commonly peaks at mid-elevations in tropical mountains (e.g., van Noort 2004;Peck et al 2008;Veijalainen et al 2014b), a pattern predicted by the "mid-domain effect" (Colwell and Lees 2000).…”

Open access in a taxonomic sense: a morphological and molecular guide to Western Palaearctic Dusona (Hymenoptera, Ichneumonidae)

“…As these species are morphologically distinct, we suggest this might be evidence either for rapid evolution or mtDNA introgression within Dusona, and thus a limitation of barcoding in separating these species. Indeed, barcoding has been shown in the past to have a limited discriminatory power in some Darwin wasp groups, such as Diplazontinae, Ichneumon Linnaeus, 1758 and Enicospilus Stevens, 1835 (Tschopp et al 2013;Klopfstein et al 2016;Shimizu et al 2020).…”

Stars in subtropical Japan: a new gregarious Meteorus species (Hymenoptera, Braconidae, Euphorinae) constructs enigmatic star-shaped pendulous communal cocoons

“…A total of 177 sequences of CO1 and 172 of 28S were compiled from GenBank. Sequences obtained from databases sometimes contain unreliable information (e.g., Klimov et al 2019;Shimizu et al 2020), and an evaluation of such sequences is always strongly recommended to ensure that the analysis is accurate. In the present study, the sequences used by Stigenberg and Ronquist (2011) and several additional sequences were considered as reliable sources.…”

“…DNA was extracted from a right mid or/and hind leg. The protocols followed from PCR to sequencing were according to the work of Shimizu et al (2020), except for the primers in Table 2, for which the PCR conditions were as follows: CO1: initial denaturation (2'00") at 95 °C, 35 cycles of denaturation (0'30") at 95 °C, annealing (0'30") at 48 °C, an extension (1'00") at 72 °C, and a final extension (10'00") at 72 °C; 28S: 1'00" at 95 °C, 40 cycles of 0'30" at 95 °C, 0'30" at 48 °C, 1'30" at 72 °C, and 5'00" at 72 °C.…”