Research Article |
Corresponding author: Jose Fernandez-Triana ( cnc.braconidae@gmail.com ) Academic editor: Gavin Broad
© 2020 Jose Fernandez-Triana, Tetsuyuki Kamino, Kaoru Maeto, Yutaka Yoshiyasu, Norio Hirai.
This is an open access article distributed under the terms of the CC0 Public Domain Dedication.
Citation:
Fernandez-Triana J, Kamino T, Maeto K, Yoshiyasu Y, Hirai N (2020) Microgaster godzilla (Hymenoptera, Braconidae, Microgastrinae), an unusual new species from Japan which dives underwater to parasitize its caterpillar host (Lepidoptera, Crambidae, Acentropinae). Journal of Hymenoptera Research 79: 15-26. https://doi.org/10.3897/jhr.79.56162
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A new species of Microgastrinae (Hymenoptera: Braconidae) parasitoid wasp, Microgaster godzilla Fernandez-Triana & Kamino, is described from Japan. From a biological and morphological perspective this is a very unusual species. It represents only the third known microgastrine to be aquatic, and the first one to be found entering the water. The female wasp searches for its hosts, aquatic larvae of Elophila turbata (Lepidoptera: Crambidae), mostly by walking over floating plants, but occasionally diving underwater for several seconds to force the larva out of its case, when it is quickly parasitized (parasitization was always observed above water). The unique searching behaviour of M. godzilla as well as its parasitization of aquatic larvae was filmed and it is presented here. The wasp has simple tarsal claws, which are elongate and strongly curved, similar to those found in the related genus Hygroplitis; they seem to represent an adaptation for gripping to the substrate when entering the water. The new species is described based on morphological, molecular (DNA barcoding), biological and ethological data. Additionally, we provide detailed diagnoses to recognize M. godzilla from all other described species of Microgaster and Hygroplitis in the Palearctic, Nearctic and Oriental regions.
aquatic parasitoid, biology, Lepidoptera, Microgastrinae, Nearctic, Oriental, Palearctic, parasitoid behaviour, taxonomy
The order Hymenoptera comprises relatively very few aquatic species, with only 150 species within 11 families (0.13% of all described Hymenoptera species) recognized so far (
The Braconidae subfamily Microgastrinae is one of the most speciose groups of parasitoid wasps, and probably the single most important group of Lepidoptera parasitoids (
Wasp specimens were reared from larvae of Elophila turbata (Butler, 1881) (Lepidoptera: Crambidae, Acentropinae) collected in ponds covered with water ferns, Azolla spp. (Salviniaceae), in several cities of the Osaka and Kyoto Prefectures, Honshu, Japan, between 2015 and 2017. The lepidopteran species was identified by one of the authors of this paper (Y. Yoshiyasu).
Emerged adult wasps were kept in laboratory conditions for observation of the wasp’s parasitization biology. Each individual female was placed in a plastic cup of approximately 30 mL volume, with moistened filter paper at the bottom of the container. The wasps were fed drops of 100% honey and kept at two different temperatures (12 °C and 25 °C).
We observed the oviposition behavior of the female wasps in a small plastic aquarium (10 × 20 × 10 cm). Twenty host larvae and one female wasp were released in the aquarium together. Observations of the wasp were taken with a Canon iVIS HF S21 video camera. The observations were repeated five times using different host and wasp individuals.
The holotype of the new species is deposited in the Osaka Prefecture University (
For the species description the morphological terms and measurements of structures are mostly as used by
Photos of the preserved specimens were taken with a Keyence VHX-1000 Digital Microscope, using a lens with a range of 13–130×. Multiple images through the focal plane were taken of a structure and these were combined to produce a single in-focus image, using the software associated with the Keyence System.
We DNA barcoded some specimens, using the standard animal locus of the 5' region of the cytochrome c oxidase I (COI) gene (
Holotype. JAPAN • ♀,
Among all described species of Microgaster this species can be distinguished because of its unique combination of morphological characters. Color patterns are distinctive, especially having all legs almost entirely yellow (only apical 0.1 of metafemur, apical 0.3 of metatibia and metatarsus are dark brown to black), tegula dark brown, pterostigma brown, and metasoma dorsally with T1–T2 black and T3+ orange-yellow. Very few Microgaster species have all coxae yellow, and then the color of the tegula and/or metasoma dorsally is usually different. Beyond color, the combination of flagellomeres with relatively distinct setae (bristly), eyes convergent ventrally, face dull due to transverse, rugose sculpture (including indication of vermiculate rugosities towards sides), notauli barely marked by impression or sculpture (and overall sculpture of anteromesoscutum with fine and relatively shallow punctures), scutellar disc mostly smooth, mesopleuron without strong crenulated sulcus, T2 and T3 about same length, T3+ smooth, all tarsi with last segment enlarged, and large but simple tarsal claws are also of diagnostic value. Microgaster godzilla shares some features with the described species of Hygroplitis, most of which also have light-coloured legs, including all coxae in many species, large tarsal claws, and last segments of tarsi enlarged. However, most Hygroplitis species have the body depressed, notauli are strongly marked, antennae have three rows of placodes and the mesopleuron has a strong, crenulated sulcus.
Although there is no available key that covers all described Hygroplitis and Microgaster, we found that all Palearctic, Nearctic and Oriental species previously described in those two genera differ from the diagnosis provided above for M. godzilla by at least one (usually more) characters. To facilitate future work on the genus we provide one-to-one comparisons of M. godzilla with every other previously described species of those two genera in the biogeographical regions relevant to the new species (see Suppl. material
Color . Head and mesosoma black; metasoma dorsally with T1–T2 black, T3+ orange-yellow; metasoma ventrally entirely orange-yellow, including hypopygium; antenna light brown; palpi orange-yellow; tegula and humeral complex dark brown; all legs almost entirely yellow (only apical 0.1 of metafemur, apical 0.3 of metatibia and metatarsus are dark brown to black); metatibial spurs white; pterostigma and most veins brown. Head. Eyes convergent ventrally; face dull due to transverse, rugose sculpture (including indication of vermiculate rugosities towards sides); frons with transverse striation; gena mostly smooth; space between ocelli with weak sculpture (a short but vague carina is barely defined); flagellomeres bristly, with relatively distinctive setae. Mesosoma. Overall sculpture of anteromesoscutum with fine and relatively shallow punctures; notauli barely marked by impression or sculpture; scutoscutellar sulcus deep and broad, with strong crenulae; scutellar disc mostly smooth, with very shallow and sparse punctures; propodeum entirely sculptured with coarse reticulation and a median, longitudinal carina; mesopleuron mostly smooth and shiny on dorsal third, mostly sculptured on ventral 0.6, without strong, crenulated sulcus; metapleuron coarsely sculptured. Metasoma. T1 and T2 strongly sculptured; T3+ smooth; T1 very broad, its width at posterior margin twice that at anterior margin, its median length 0.9 its width at posterior margin; T2 rectangular and about same length as T3; hypopygium mostly inflexible, with a weakly defined and small fold apico-ventrally; ovipositor sheaths with relatively long setae the setose part roughly half the length of metatibia. Legs. All legs with simple and large tarsal claws; all tarsi with last segment enlarged. Wings. Fore wing with relatively large and quadrangular areolet, vein R1 longer than pterostigma length, vein r longer than vein 2RS and much longer than areolet height, vein r arising beyond mid point of pterostigma; hind wing with vannal lobe entirely setose. Body measurements (in mm). Body length: 3.3; fore wing length: 3.2; ovipositor sheath length 1.28; metatibia length 0.62; metafemur length/width: 0.99/0.28; flagellomere 2 length/width: 0.26/0.07; flagellomeres 13+ missing in the two female specimens (holotype and one paratype) available to JFT for study and species description.
The species has only been collected in the prefectures of Osaka and Kyoto in Honshu, Japan.
Microgaster godzilla sp. nov. has been reared from Elophila turbata (Butler, 1881) (Lepidoptera: Crambidae, Acentropinae), whose larvae are aquatic. Each larva constructs a portable case from fragments of aquatic plants (e.g. Azolla spp., Trapa spp. and Spirodela spp.) and lives inside the case which is found slightly above or slightly under the water surface (
Four DNA barcodes were obtained (two of them almost full length at 631 bp, the other two specimens rendered partial barcodes of 421 bp each). Those sequences correspond to BIN BOLD:ADO8283 and are unique among all available sequences of Microgastrinae in BOLD, with the closest BIN (an undescribed Microgaster species from Papua New Guinea) differing by 34 bp (5.2%) (Suppl. material
The species is named after Godzilla (Japanese: ゴジラ, Hepburn: Gōjira), a fictional monster (kaiju) that became an icon after the 1954 Japanese film of the same name and many films afterwards. The wasp name is intended to respectfully honour one of the most recognizable symbols of Japanese popular culture worldwide. The wasp’s parasitization behaviour bears some loose resemblance to the kaiju character, in the sense that the wasp (after diving underwater to search for its host, a moth caterpillar) suddenly emerges from the water (to parasitize the host), similar to how Godzilla suddenly emerges from the water in the movies. Additionally, Godzilla has sometimes been associated, albeit in different ways, with Mothra (Japanese: モスラ, Hepburn: Mosura) another kaiju that is typically portrayed as a larva (caterpillar) or adult moth.
There is some evidence that Hygroplitis may just be a species-group of Microgaster (
Microgaster godzilla sp. nov. could be considered to be intermediate between those two genera but is not the first Microgaster reported to be like that. Another species, Microgaster deceptor Nixon, 1968, has similar simple tarsal claws which are relatively large, and it was also considered as intermediate between Hygroplitis and Microgaster by
This study was supported in part by a grant from JSPS KAKENHI (No. 19H00942) to KM and by project 3199 “Systematics of beneficial arthropods in support of resilient agroecosystems”, from Agriculture and Agri-Food Canada. Andrew Bennett (
Wasp parasitization behaviour including diving underwater
Data type: multimedia
Wasp parasitization behaviour above water
Data type: multimedia
Probing with antennae above water
Data type: multimedia
Neighbor Joining tree of all DNA barcode sequences
Data type: molecular data
Explanation note: Neighbor Joining tree of all DNA barcode sequences of Microgaster and Hygroplitis species in BOLD (http://www.boldsystems.org/) with more than 400 base pairs as of June 2020.
Differences between Microgaster godzilla and other Hygroplitis and Microgaster species
Data type: species data
Explanation note: Differences between Microgaster godzilla and other Hygroplitis and Microgaster species, arranged in alphabetical order.