Mycophagous Gall Midges (Diptera: Cecidomyiidae) in Korea: Newly Recorded Species with Discussion on Four Years of Taxonomic Inventory

Anim. Syst. Evol. Divers. Vol. 36, No. 1: 60-77, January 2020 https://doi.org/10.5635/ASED.2020.36.1.055 Review article Mycophagous Gall Midges (Diptera: Cecidomyiidae) in Korea: Newly Recorded Species with Discussion on Four Years of Taxonomic Inventory Daseul Ham1, Mathias Jaschhof 2, Yeon Jae Bae3,* 1Korean Entomological Institute, Korea University, Seoul 02841, Korea 2Station Linné, Ölands Skogsby 161, SE-38693 Färjestaden, Sweden 3Division of Environmental Science and Ecological Engineering, College of Life Sciences, Korea University, Seoul 02841, Korea ABSTRACT Cecidomyiidae (Diptera) consists of six subfamilies, which are divided into three groups according to larval ecological habits (phytophagous, mycophagous, and zoophagous). The five basal subfamilies of Cecidomyiidae consist entirely of mycophagous species, with approximately 1500 species described worldwide and 29 previously known to occur in Korea. In this study, 37 named species (1 Lestremiinae, 29 Micromyinae, 4 Winnertziinae, and 3 Porricondylinae species) are newly reported from South Korea. We excluded Lestremia yasukunii Shinji from the list of Korean mycophagous cecidomyiids as it is a nomen nudum. Therefore, we herein officially recognize 65 species, 30 genera, and four subfamilies for the Korean mycophagous cecidomyiid fauna. We also provide diagnoses and photographs to aid species identification and discussion on the four years of gall midge taxonomic inventory in South Korea. Keywords: ‌Cecidomyiidae species new to Korea, taxonomic diagnosis, gall-midge taxonomy, insect identification, Korean gall-midge fauna, Korean indigenous species survey INTRODUCTION Sweden (Jaschhof, unpublished data). The Swedish fauna of fungus-feeding gall midges has been, for nearly 15 years, the Cecidomyiidae (gall midges) is well-known as a family of subject of intensive taxonomic inventory work (e.g., Jaschhof plant-feeders; however, it also contains many predatory and and Jaschhof, 2009, 2013), and, as a result, it may be regard- mycophagous species. Unlike many other insect groups, in- ed as the best-studied national fauna worldwide. At a higher cluding gall-inducing insects and other plant-feeding gall level, the family Cecidomyiidae is possibly currently the most midges, mycophagous cecidomyiids are exclusively studied species-rich family of Diptera, with an estimated 2,000,000 by professional researchers. No amateur entomologist is in- species (Hebert et al., 2016). More than 800 species of Ce- terested in these tiny, elusive midges, nor in their faunistic cidomyiidae were recorded from one site at a Neotropical aspects. It is fair to say that mycophagous gall midges are cloud forest, rendering this family the most speciose of all the probably the most poorly researched, large subgroup of the dipteran families recorded there (Borkent et al., 2018; Brown order Diptera. In contrast, it is known that mycophagous cec- et al., 2018). ids occur worldwide - especially in woodlands - and that they The mycophagous Cecidomyiidae are classified into five are so speciose that the number of species in specific regions subfamilies, namely Catotrichinae, Lestremiinae, Micromy- or worldwide is impossible to estimate. There are currently inae, Winnertziinae, and Porricondylinae (the sixth subfamily, ~1,500 named species of mycophagous cecidomyiids in the Cecidomyiinae, contains all the herbivorous and predatory world, comprising approximately one-fourth of all Cecido- species). Micromyinae, with 38 extant genera and 579 extant myiidae (Gagné and Jaschhof, 2017). Of these, 560 species species, and Porricondylinae, with 84 extant genera and 501 have been recorded in only one country in northern Europe: extant species, are the most diverse fungus-feeding subfam- This is an Open Access article distributed under the terms of the Creative *To whom correspondence should be addressed Commons Attribution Non-Commercial License (http://creativecommons.org/ Tel: 82-2-3290-3408, Fax: 82-2-3290-3623 licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, E-mail: [email protected] and reproduction in any medium, provided the original work is properly cited. eISSN 2234-8190 Copyright The Korean Society of Systematic Zoology Mycophagous Gall Midges in Korea ilies (Gagné and Jaschhof, 2017). Most of these genera and lished report) are documented in publications (e.g., Jaschhof, species were discovered and named from the Palearctic re- 2000, 2001). In summary, it can be stated that no long-term, gion, as Europe has traditionally been the center of taxonomic concerted effort has ever been made to investigate the Far studies and a home base for the research of faunas from oth- Eastern hotspot systematically. Consequently, we have only er continents (cf. Jaschhof and Jaschhof, 2009: 18ff.; 2013: vague ideas of the faunal size and composition in that region. 22ff.). Moreover, tools for species identification, such as specimen The biology of the midges in question is even more insuffi- collections, published descriptions and keys, and DNA bar- ciently researched than their taxonomy. Their larvae, which is code libraries, are of limited use because of incomplete spe- the ontogenetic stage occupied with feeding (adults usually do cies coverage and unsatisfactory quality (see Discussion). not assimilate food), are described for only a small proportion Clearly, the Far Eastern Palearctic is the place to perform pio- of the named species. Details regarding host (fungus) special- neer work for scholars focused on mycophagous cecids. ization, habitat requirements, and interactions with other spe- Korea was a blank spot on the world map of mycophagous cies are poorly understood. Larvae are usually found in asso- cecid diversity until 2003, when a species of Mycophila Felt ciation with plant litter, with soil and rotting wood being the (in Micromyinae) was reported as a pest infesting mushroom most common larval habitats. Furthermore, larvae are gener- cultivations (Lee and Kim, 2003). Two similar cases, but re- ally considered to pierce and suck fungal hyphae penetrating garding the genus Camptomyia Kieffer (in Porricondylinae), plant detritus (Mamaev and Krivosheina, 1965). Their eco- were reported by Shin et al. (2011). Eventually, a taxonomic logical role is, therefore, best described as mycophagous de- inventory focused on the mycophagous subfamilies of Ce- tritobiont, or in more general terms, detritivores. Krivosheina cidomyiidae was started in 2016 as part of the framework (2006) reviewed the ecology of bark- and wood-dwelling program “Korean Indigenous Species Survey-Insects,” ini- (xylobiont) species in an evolutionary context. However, tiated by the National Institute of Biological Resources in much remains unknown regarding the biology of adults, Incheon, South Korea (https://www.nibr.go.kr/cmn/sym/mnu/ which is the ontogenetic stage commonly used for species mpm/512010000/enHtmlMenuView.do). Since then, a total identification. Moreover, the classification of mycophagous of 29 species have been recorded as occurring in the country Cecidomyiidae is largely based on interpretation from adult (Ham and Bae, 2017; Ham et al., 2018, 2019; Jaschhof et morphology, with males having an advantage over females al., 2018), Lestremia yasukunii Shinji, a dubious name that in providing data for taxonomic and phylogenetic interpreta- was herein deleted from the Korean checklist (cf. Gagné and tion (Jaschhof and Jaschhof, 2009, 2013). In recent years, an Jaschhof, 2017), not included. integrated approach using both morphological and molecular In the present paper, we document findings of 37 additional data has been increasingly applied to species delimitation (e.g., species, namely 1 Lestremiinae, 29 Micromyinae, 4 Winnert- Jaschhof, 2016b) and phylogeny reconstruction (Sikora et al., ziinae, and 3 Porricondylinae. This more than doubles the 2019). number of species recorded from Korea, which now stands The realization that the Far East of the Palearctic region is a at 66. Besides these species, we are aware of the existence hotspot of mycophagous cecid diversity has developed grad- of twice as many species among the material that we cannot ually since the 1970s, initiated by studies by Boris M. Ma- name at this stage, either because the available literature is maev in Far Eastern Russia (many different articles, see list in not sufficient for a positive identification or because they are Gagné and Jaschhof, 2017) and Junichi Yukawa in Japan (e.g., unnamed. Yukawa, 1971). Additional data have been published since the 1990s by Wenjun Bu and subsequent authors in China. At the beginning of the 2000s, the Russian researcher Zoya MATERIALS AND METHODS A. Fedotova started publishing on mycophagous cecids from Far Eastern Russia (cf. Gagné and Jaschhof, 2017, for a list of The number of male specimens and species as examined ma- her articles) and authored the Cecidomyiidae chapter in the terials used here are 80 and 37. All samples were collected famed Keys to the Insects of the Russian Far East (Fedotova, using malaise traps in 2019, except for two, which were col- 2004). The latter publication is still the most comprehensive lected in Cheongsong-gun, 2017 by sweep net and Sangju- review available on mycophagous cecid diversity in the Far si, 2018 by malaise trap. Gangwon-do (Mt. Odaesan, Mt. Eastern Palearctic, even though it is of limited suitability for Gariwangsan) and Gyeongsangbuk-do (Cheongsong-gun, species identification (see Discussion). One of us, MJ, studied Sangju-si) were investigated

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