Regular Article pISSN: 2288-9744, eISSN: 2288-9752 J F E S Journal of Forest and Environmental Science Journal of Forest and Vol. 35, No. 4, pp. 258-262, December, 2019 Environmental Science https://doi.org/10.7747/JFES.2019.35.4.258 Biological Characteristics of Dolichomitus cephalotes and Dolichomitus curticornis (, ), Parasitoids of Monochamus saltuarius (Coleoptera, Cerambycidae)

Tae-Woong Jang1, Jong-Chul Jeong2, Jin-Kyung Choi3, Chan-Sik Jeong4 and Jong-Kuk Kim1,* 1Department of Forest Science, Kangwon National University, Chuncheon 24341, Republic of Korea 2Korea National Park Research Institute, Wonju 26441, Republic of Korea 3Department of Science Education, Daegu National University of Education, Daegu 42411, Republic of Korea 4Korea Forest Service, Inter-Korean Forest Cooperation, Daejeon 35208, Republic of Korea

Abstract This study was aimed to clarify the morphological and ecological characteristics of Dolichomitus cephalotes and Dolichomitus curticornis in order to provide basic data to be used for biological control against Monochamus saltuarius. D. cephalotes and D. curticornis are univioltine in the central region of Korea and overwinters as larval stage inside the cocoon. Both species are ectoparasitoid, and a solitary parasitoid. D. cephalotes adults are emerged from the beginning of April to the middle of May, while D. curticornis adults are emerged from late April to mid-May.

Key Words: parasitoid, Monochamus saltuarius, genus Dolichomitus, pine wilt disease, biological control

Introduction problems, researches to find out environmentally friendly measures have been carried out, and as a result, various nat- Pine wilt disease was first found in Mt. Geumjungsan in ural enemies have been identified. In this process, some 1988, and has been continuously causing damages to pine species of the Genus Dolichomitus were identified as one of tree, black pine tree and Korean pine forest in Korea the prime natural enemies, which can be applied to control (Teramoto et al. 2014; Korea Forest Service 2016; Park et the density of the and Monochamus saltuarius and al. 2016; Ha and Lee 2017). In order to prevent and con- Monochamus alternatus (Kim et al. 2010). trol the disease, various control methods have been im- Genus Dolichomitus belongs to the tribe of plemented in a comprehensive manner, but measures are the family Ichneumonidae, Hymenoptera. It is first re- highly relying on chemical method (Korea Forest Service ported by Smith (1877) and currently 70 species are 2016). Some of measures have been identified as effective recorded. Among them, 17 species have been are recorded for controlling pine wood nematodes, but which are known in Korea up to date (Choi et al. 2016). The ecology and host to have inherently negative effects in terms of maintaining range of Dolichomitus species inhabited in Korea is not of integrity and economical aspect. In order to solve these known, but in overseas, it is known as key natural enemies

Received: July 24, 2019. Revised: November 15, 2019. Accepted: November 20, 2019.

Corresponding author: Jong-Kuk Kim

Department of Forest Science, Kangwon National University, Chuncheon 24341, Republic of Korea Tel: 82-33-250-8363, Fax: 82-33-259-5617, E-mail: [email protected]

258 Journal of Forest and Environmental Science http://jofs.or.kr Jang et al.

of boring , for example, Cerambycidae and för Entomologi, Stockholm, Sweden; TMA_Termeszettudomanyi Buprestidae (Smith et al. 2003; Kenis and Hilszczanski Muzeum Allattara, Budapest, Hungary. 2007). Various species of Dolichomitus have been identi- Occurrence, life span, sex ratio and Life cycle fied as parasitoids in Monochamus that mediates pine wood nematode (Soper and Olson 1963; Naves et al. 2005; Gima The trees in which M. saltuarius were collected at the be- 2011; Varga 2012). ginning of March, 2011 and 2012 from the pine forests in The purpose of this study is to examine the morpho- Gajungri- and Gwangpan-ri in Chuncheon-si, Yongdam-ri logical features of the two species, D. cephalotes and D. in Hwacheon-gun, and Songhyun-ri of Yanggu-gun, curticornis, providing the basic data for the biological con- Korea. After a parasitic tree was prepared to a length of 1 m, trol of the parasitic natural enemies. We also investigated to it was placed in a growing cage (with iron net: 1 m×1 investigate the growth, sex ratio, life cycle, and adult life m×1.5 m). The population of female and male of D. ceph- span of these two species. alotes and D. curticornis were investigated by each stage from April, when they moved away from the wood samples. Materials and Methods In addition, when the adults leave from the wood samples, they are collected on the day and released in cages (made of Morphology acryl 45 cm×45 cm×45 cm). Then a crude honey was fed, Materials used in this study were collected in and was cultivated indoors to check their life span. Gangwon-do, South Korea (Fig. 1). Morphological termi- nology follows mostly that of Townes (1690). Specimens Results and Discussion were examined using an AxioCam MRc5 camera attached Description to a stereo microscope (Zeiss SteREO Discovery. V20; Carl Zeiss, Gotingen, Germany), processed using Axio Family Ichneumonidae Latreille, 1802 Vision SE64 software (Carl Zeiss), and optimized with a Subfamily Wesmael, 1845 Delta imaging system ( I-solution Inc. Vancouver, Canada). Genus Dolichomitus Smith, 1877 Distributional data mainly follow that of Yu et al (2012). Dolichomitus cephalotes (Holmgren, 1860) Descriptions are based on South Korean specimens. Ephialtes cephalotes Holmgren, 1860: 1-76. Type: fe- Collection abbreviations: CNC_Canadian National male; type locality: Sweden; type depository: NR. Collections, Agriculture & Agri-Food Canada, Ottawa, Ephialtes longicauda Mocsary, 1897: 644-647. Type: fe- Ontario, Canada; NR_Naturhistoriska Riksmuseet, Sektionen male; type locality: Hungary; type depository: TMA. Ichneumon (Exeristoidea) watsoni Viereck, 1924: 202.

Fig. 2. Dolichomitus cephalotes. (a) larva, (b) male and female pupa, (c) fe- Fig. 1. Location of collecting site. male adult.

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Type: female; type locality: Canada_Quebec; type depos- Larva: Larvae of this species were observed from late itory: CNC. March to late July. It was confirmed that the mature larvae (13.9±0.9 mm) developed during the larval stages by Diagnosis. Body 17-20 mm; fore wing 16-19 mm; ovi- moulting 3-4 times. The body color of larva is milky white. positor 80-100 mm long. Body shape is maggot form and head and apical abdominal Body black. Palpi dark brown; tegula yellow. All legs segments are more slender than the middle part of reddish brown except hind tibia and tarsi blackish brown. abdomen. After the middle of July, cocoon (23.4±3.3 mm) Antenna with 37-40 flagellomeres. was built and wintered in prepupa state. It putated around Head angular, not narrowed behind eyes in dorsal view. the middle of March of the following year and was emerged Frons polished with transversal wrinkles. Lower tooth lon- the middle of April (Pupa length: 17.0±0.4 mm (female); ger than upper tooth. Pronotum polished and smooth. 14.3±0.6 mm (male)). Speculum convex and glabrous. Prepectal carina extending above corner of pronotum and curved forward, not reach- Host records: [Coleoptera: Cerambycidae] Monochamus ing anterior margin of mesopleuron. Propodeum reticulate. sartor, Monochamus sutor, Monochamus ussurovi, Monochamus Fore tibia with thin setae on the middle of inside surface. saltuarius (new record), [Hymenoptera: Xiphydriidae] Fifth hind tarsus as long as third. First and second tergites Xiphydria camelus (Yu et al. 2016). slightly elongate, third tergite quadrate (Figs. 2, 3). Distribution: South Korea (new record), Austria, Bulgaria, Canada, China, Czech Republic, Germany, Hungary, Netherlands, Poland, Romania, Russia, Spain, Sweden, Switzerland, Ukraine, United Kingdom (Yu et al. 2016).

Dolichomitus curticornis (Perkins 1943) Ephialtes curticornis Perkins, 1943: 249-273. Type: unknown. Diagnosis. Body 14-22 mm; fore wing 9-15 mm; ovipo- sitor 14.5-25 mm long. Body black. Palpi and tegula yellow. Fore and mid coxae reddish yellow, darkened basally; fore and mid femur red- dish yellow; fore and mid tibiae and trochanters yellow; hind leg almost black except trochanters and femur reddish brown. Antenna with 25-29 flagellomeres. Fig. 3. Dolichomitus spp. (a) Head in frontal view of D. cephalotes, (b) hab- itus of D. cephalotes in lateral view, (c) Head in frontal view of D. curticornis, Head angular, not narrowed behind eyes in dorsal view. (d) habitus of D. curticornis. Scale bars: 5 mm=b, d; 0.5 mm=a, c. Frons polished with transversal wrinkles. Lower tooth lon-

Fig. 4. Dolichomitus curticornis. (a) male pupa , (b) female pupa, (c): female adult.

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ger than upper tooth. Pronotum with wrinkles on ventral April to the beginning of May in 2012. 50% cumulative area. Speculum convex and glabrous. Prepectal carina ex- adult eclosion rate was appeared in mid-April and late tending above corner of pronotum and curved forward, April. 50% cumulative adult eclosion rate was appeared in reaching anterior margin of mesopleuron. Propodeum with early May and late April (Fig. 5). The period of growth was weak median longitudinal carinae; areola and petiolar areas relatively short in both species, and the season of adult eclo- granulate, and the rest of propodeum rugosely punctate sion rate was somewhat different in each given year. These with wrinkles. Fore tibia with thin setae on the middle of in- differences seem to be attributed to different climate envi- side surface. Fifth hind tarsus shorter than third. First and ronment in their respective habitat. The ratio of females D. second tergites elongate, third tergite quadrate (Figs. 3, 4). cephalotes and D. curticornis was 48.9-61.5% and 50.0- Larva: Larvae of this species were observed from the 55.3%, respectively. The life span of female and male D. middle of April to the middle of July. From the first part of cephalotes was 13.2±2.7 days and 6.8±2.0 days, July, cocoon (25.6±2.5 mm) was built and wintered in pre- respectively. The females have longer lifespan than males. pupa state. It putated around the late February of the fol- The mean lifespan of D. curticornis was 11.8±2.6 days, lowing year and was emerged the first part of April (Pupa and that of males was 8.1±3.0 days. In the outdoor raising length: 20.9±0.7 mm (female); 19.3±0.6 mm (male)). population, the life span of the female and male was some- Host records: [Coleoptera: Buprestidae] Anthaxia aurulenta, what longer than that of the indoor raising population. It is [Coleoptera: Cerambycidae] Molorchus minor, Monochamus salt- reported that the average lifespan of adult larva of the allied uarius (new record), [Lepidoptera: Gelechiidae] Exoteleia dode- species, D. populneus, was 6.3 days (Tsankov and Georgiev cella, [Lepidoptera: Tortricidae] Rhyacionia buoliana, Rhyacionia 1991) and honey, pollen and sugar water are known to en- resinella, [Hymenoptera: Siricidae] Sirex cyaneus dux, Urocerus hance the number of spawning and lifespan of adult para- argonautarum, [Hymenoptera: Xiphydriidae] Xiphydria cam- sitic predators (Syme 1975; Jervis and Kidd 1999). elus (Yu et al. 2016). Life cycle Distribution: Austria, Belarus, Belgium, Bulgaria, Croatia, Czech Republic, Finland, France, Germany, Greece, D. cephalotes were emerged from the beginning of April Hungary, Latvia, Poland, Romania, Russia, South Korea, to the middle of May, and after the 2nd to 3rd day of emer- Spain, Sweden, Switzerland, Ukraine, Yugoslavia (Yu et al. gency, it spawned on last instar larva and pupa of M. salt- 2016). uarius as ectoparasitoid, and it was a solitary parasitoid. Eggs were laid from late April to late May, larvae devel- Occurrence, life span, sex ratio of larva oped with four times of molting from the beginning of May The adult emergence of D. cephalotes was from the begin- to the end of June. From late May, cocoon-making pop- ning of April to the middle of May in 2011, and from mid ulation emerged and wintered in prepupa state, and then of April to early May in 2012. 50% cumulative adult eclo- larva molting was started from mid-February. D. curti- sion rate was appeared in mid-April and late April, whereas cornis was emerged from the end of April to the middle of the adult emergence of D. curticornis from the beginning of May, and became ectoparasitoid and solitary parasitoid that May to the middle of May in 2011, and from the end of spawned on last instar larva and pupa. Larvae were ob-

Fig. 5. Seasonal occurrence of D. cephalotes and D. curticornis in 2011-2012. (a) D. cephalotes, (b) D. curticornis.

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