Monochamus saltuarius Gebler (Coleoptera, Cerambycidae) serves as the primary carrier of Bursaphelenchus xylophilus (Steiner &amp;amp; Buhrer) (Aphelenchida, Aphelenchoididae) in the middle-temperate zone of China. Pine wilt disease caused by B. xylophilus leads to serious losses to pine forestry around the world. It is necessary to study the biological control of M. saltuarius to effectively prevent the further spread of B. xylophilus. To explore the insect resources that act as natural enemies of M. saltuarius, investigations were conducted on natural enemy insects by splitting Pinus koraiensis Siebold &amp;amp; Zucc (Pinales, Pinaceae) damaged by M. saltuarius and dissecting their trunks in Yingpan Village, Fushun County, Fushun City, Liaoning Province, China, in 2023. A larva of Inocellia (Amurinocellia) calida (H. Aspöck &amp;amp; U. Aspöck) (Raphidioptera, Inocelliidae) was discovered in the trunk of an infested P. koraiensis. Additionally, the feeding habits of I. calida were preliminarily examined under indoor conditions and a description of its morphological characteristics was provided. When placed in an indoor environment, the I. calida larva began pupating after a period of 21 days, during which time it consumed and attacked a total of 23 M. saltuarius larvae. Ultimately, after a pupal period of ten days, the I. calida larva emerged successfully as an adult. This discovery marks the first recorded presence of I. calida in Liaoning Province and the first documentation of I. calida in China, serving as a natural predatory enemy of M. saltuarius

Jue Wang

Miao Yu

Shiyu Kuang

Wenfeng Yan

Yanan Zheng

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Biodiversity Data Journal 12: e114294doi: 10.3897/BDJ.12.e114294 Research Article Inocellia (Amurinocellia) calida (Raphidioptera,Inocelliidae) was first observed as a predator of Monochamus saltuarius (Coleoptera,Cerambycidae) in China, the vector of Bursaphelenchus xylophilus (Aphelenchida,Aphelenchoididae)Miao Yu , Jue Wang , Wenfeng Yan , Shiyu Kuang , Yanan Zheng‡ College of Forestry, Shenyang Agricultural University, Shenyang, ChinaCorresponding author: Yanan Zheng (rockyya@163.com)Academic editor: Vinicius S. FerreiraReceived: 17 Oct 2023 | Accepted: 08 Jan 2024 | Published: 17 Jan 2024Citation: Yu M, Wang J, Yan W, Kuang S, Zheng Y (2024) Inocellia (Amurinocellia) calida (Raphidioptera,Inocelliidae) was first observed as a predator of Monochamus saltuarius (Coleoptera, Cerambycidae) in China,the vector of Bursaphelenchus xylophilus (Aphelenchida, Aphelenchoididae). Biodiversity Data Journal 12:e114294. https://doi.org/10.3897/BDJ.12.e114294AbstractMonochamus saltuarius Gebler (Coleoptera, Cerambycidae) serves as the primary carrierof Bursaphelenchus xylophilus (Steiner & Buhrer) (Aphelenchida, Aphelenchoididae) in themiddle-temperate zone of China. Pine wilt disease caused by B. xylophilus leads to seriouslosses to pine forestry around the world. It is necessary to study the biological control of M.saltuarius to effectively prevent the further spread of B. xylophilus. To explore the insectresources that act as natural enemies of M. saltuarius, investigations were conducted onnatural enemy insects by splitting Pinus koraiensis Siebold & Zucc (Pinales, Pinaceae)damaged by M. saltuarius and dissecting their trunks in Yingpan Village, Fushun County,Fushun City, Liaoning Province, China, in 2023. A larva of Inocellia (Amurinocellia) calida(H. Aspöck & U. Aspöck) (Raphidioptera, Inocelliidae) was discovered in the trunk of an‡ ‡ ‡ ‡ ‡© Yu M et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0),which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.infested  P. koraiensis.  Additionally,  the  feeding  habits  of  I. calida were  preliminarilyexamined under indoor conditions and a description of its morphological characteristicswas provided. When placed in an indoor environment, the I. calida larva began pupatingafter a period of 21 days, during which time it consumed and attacked a total of 23 M. saltuarius larvae. Ultimately, after a pupal period of ten days, the I. calida larva emergedsuccessfully as an adult. This discovery marks the first recorded presence of I. calida inLiaoning Province and the first documentation of I. calida in China, serving as a naturalpredatory enemy of M. saltuarius.KeywordsInocellia (Amurinocellia) calida, Monochamus saltuarius, morphology characters, feedinghabitIntroductionPine wilt  disease is  a worldwide forest  disease caused by Bursaphelenchus xylophilusSteiner & Buhrer (Aphelenchida, Aphelenchoididae) (Mamiya and Kiyohara 1972, Zhao etal. 2008) which has been listed as a quarantine pest in more than 40 countries (Tóth 2011).Bursaphelenchus xylophilus is  currently  distributed in  China,  Korea,  Japan,  the  UnitedStates, Portugal and other countries (Mota and Vieira 2009). Bursaphelenchus xylophiluscan cause devastating damage to pine forest ecosystems and biodiversity in infected areasand serious economic losses (Ye 2019).  Although B. xylophilus is  seriously  harmful,  itcannot spread by itself  and needs to be transmitted through wounds caused by vectorinsects  feeding  and  oviposition  (Fan et  al.  2021).  Monochamus saltuarius Gebler(Coleoptera, Cerambycidae) is the vector insect of the B. xylophilus in Japan (Heisuke etal. 1987), Korea (Kwon et al. 2006) and the mid-temperate region of China (Fan et al.2021) and carries B. xylophilus that spread causing a large number of pine trees to die.The use of  natural  enemies for  biological  control  is  recognised as one of  the effectivecontrol  techniques (Tang et  al.  2011) and, as the prerequisite for this is to identify thespecies of natural enemies, it is necessary to carry out surveys of natural enemies. Severalpredatory natural enemies of M. saltuarius have been documented, including Stenagostus umbratilis (Coleoptera,  Elateridae),  Trogossita japonica (Coleoptera,  Trogossitidae),Thanasimus lewisi (Coleoptera,  Cleridae)  and  Kolibacia squamulata (Coleoptera,Trogossitidae). In addition to these predators, seven parasitic natural enemies have beenidentified,  namely  Cleonymus serrulatus (Hymenoptera,  Pteromalidae),  Dolichomitus cephalotes (Hymenoptera, Ichneumonidae), D. curticornis (Hymenoptera, Ichneumonidae),D. nakamurai (Hymenoptera,  Ichneumonidae),  Echthrus reluctator (Hymenoptera,Ichneumonidae), Dastarcus helophoroides (Coleoptera, Bothrideridae) and Rhimphoctona lucida (Hymenoptera,  Ichneumonidae).  Furthermore,  several  unidentified species of  thegenus Spathius (Hymenoptera,  Braconidae)  are  known  to  parasitise  M. saltuarius.However,  this  number remains lower  compared to  the 27 species of  predatory naturalenemies and 22 species of parasitic natural enemies recorded for M. alternatus (Zhang et2 Yu M et alal.  2022). Therefore, further exploration and investigations are imperative to discover amore extensive range of natural enemy insect resources.The  species  Inocellia ( Amurinocellia)  calida (H.  Aspock  &  U.  Aspock)  (Raphidioptera,Inocelliidae) (Aspöck and Aspöck 1973), which was discovered in this study, belongs to thefamily Inocelliidae within the order Raphidioptera (Engel 2002). This order is characterisedby having the fewest number of species amongst fully metamorphosed insects (Oswaldand  Machado  2018).  All  extant  snakeflies  of  the  Raphidioptera  are  found  only  in  theNorthern  Hemisphere  (Oswald  2022).  Inocelliidae  are  holometabolous  terrestrial  andarboreal insects, with carnivorous larvae and adults, making it a rare and valuable species(Oswald 2022, Yang and Liu 2022). Previous research on I. calida is limited, with only afew reports indicating its distribution in China (Jilin Province), North Korea, South Koreaand the Far East region of Russia (Liu et al. 2009). However, the life history and feedinghabits are not reported.This  study  is  the  first  to  report  that  I. calida is  a  predator  of  M. saltuarius in  China.Additionally, ecological information and specimen photos of I. calida were presented.Material and Methods Insect collectionIn March 2023, P. koraiensis infected by B. xylophilus and its vector M. saltuarius were cutinto  one-metre-long logs  in  Yingpan Village,  Fushun County,  Liaoning  Province,  China(41°56′17″N, 124°12′17″E, 140 m altitude, 823 mm annual average precipitation). Theselogs were then dissected to investigate and collect the natural enemies of M. saltuarius.The number of M. saltuarius collected in each log, as well as the natural enemy insectsand their predation status, were recorded.Identification and photography We only found one female of I. calida,  its examination being carried out using a ZeissStemi508 stereomicroscope and the species identification was based on naturally driedspecimens. Specimens were photographed using a Nikon D610 camera and Tuli 100 mmF2.8  lens.  The  species  of  natural  enemy  insects  were  identified  using  morphologicalmethods (Liu et al. 2009, Shen et al. 2022).Study on the feeding habits of Inocellia calidaFor the insect-raising experiment, logs of P. koraiensis measuring 100 × 50 × 50 mm wereused. A middle groove with dimensions of 30 × 10 × 10 mm was carved into one side ofeach log. Larvae, pupae and adults of M. saltuarius were placed in the grooves of theinsect-raising logs, while I. calida larvae were placed in separate logs. These two sets oflogs were then placed inside a transparent plastic box (Zhang et al. 2008). To maintainInocellia (Amurinocellia) calida (Raphidioptera, Inocelliidae) was first ... 3humidity levels, the box was supplemented with water-soaked absorbent cotton, which wasregularly replaced (Fig. 1). During the experiment, one larva of M. saltuarius was providedas prey for the I. calida larvae each time. After the consumption of the M. saltuarius larva, anew one was introduced.  The predation behaviour  of  I. calida larvae on M. saltuariuslarvae was observed daily and the predation ability and the quantity of prey consumed by I.calida were recorded.ResultsInocellia (Amurinocellia) calidaInocellia (Amurinocellia) calida H. Aspöck & U. Aspöck, 1973: 47. Type locality: Russia(Khabarovsk in Amur-Region).Female: Body length 12.90 mm, body width 2.60 mm, wing length 26.04 mm (Fig. 2).Feeding habitThe larva of I. calida (Fig. 3A) from the Dahuofang Forest presented remarkable activity, byrapidly locating and either preying upon or biting M. saltuarius larvae within the worm-hole(Fig. 4). The larva of I. calida were collected on 27 March 2023 and, throughout its 21-dayartificial feeding larval phase, it predominantly engaged in feeding and excreting during thenight-time, capturing or biting a total of 23 M. saltuarius larvae. Of these, 16 larvae werepreyed upon and seven larvae were bitten. During the indoor rearing phase, the larvae of I.calida underwent one moulting process on 16 April  2023 (Fig.  3B).  Its pupation periodFigure 1.  Artificial  rearing  of  Inocellia (Amurinocellia)  calida.  Including  the  wood  for  raising  insects,groove for placing Monochamus saltuarius larvae, and absorbent cotton. 4 Yu M et alspanned 10 days and turned into an adult on 26 April 2023. Post-emergence (Fig. 3C), itlived for 17 days and died on 16 May 2023. Based on the observations made during theartificial feeding of I. calida and the number of larvae it attacked, it became evident that I. calida plays a substantial  role  as a predatory antagonist  to  M. saltuarius.  It  exhibits  asignificant predation rate, frequently directly consuming M. saltuarius larvae (Fig. 5A) orpuncturing their epidermis to extract bodily fluids. In certain cases, a single M. saltuariuslarva displayed as many as 29 bite marks on its body surface (Fig. 5B).DiscussionPrevious research has indicated that Inocelliidae are predatory insects with a broad preyrange (Aspöck et al. 1991). Inocelliidae larvae typically inhabit bark and primarily feed onFigure 2.  Inocellia (Amurinocellia) calida female. A dorsal aspect; B head, dorsal aspect; C fore wing. Figure 3.  Photographs of Inocellia (Amurinocellia) calida during development. A larva; B the exuvia ofthe larva; C an adult. Inocellia (Amurinocellia) calida (Raphidioptera, Inocelliidae) was first ... 5various insects, including Coleoptera, Lepidoptera and Hymenoptera, as well as the eggsand larvae of  Collembola,  mites and spiders (Kovarik et  al.  1991,  Aspöck and Aspöck 2009). However, there is currently a lack of research on the feeding habits and quantity ofInocelliidae. In this study, over a 21-day period of larva observation, I. calida larvae preyedupon  and  bit  23  M. saltuarius larvae.  Comparatively,  Cryptalaus berus (Coleoptera,Elateridae),  a  predator  of  M. alternatus,  preyed  upon  and  bit  27  M. alternatus larvaethroughout its entire 130-day developmental period (Zhang et al. 2008). This indicates thatI. calida exhibits a higher feeding rate. Given its extended larval development period, I. calida has the potential to be an effective biocontrol agent against M. saltuarius.Figure 4.  Inocellia (Amurinocellia) calida preying on the larva of Monochamus saltuarius. Figure 5.  The dead larva of Monochamus saltuarius. A preyed larva of Monochamus saltuarius; B thebitten larva of Monochamus saltuarius. 6 Yu M et alPrevious studies have documented that Inocelliidae larvae undergo 10-11 instars (Aspöcket al. 1991). In this study, the I. calida larva was fed for 21 days, but as it was already alarva when collected, its exact larval period could not be accurately determined. I. calidahas a pupal period of 10 days and an adult period of 17 days. Since the larvae in this studymoulted once and then began pupation in the pupal chamber within the insect-raising log, itcan be inferred that they were in their final instar at the time of collection and have beenactively preying before reaching that stage. Most Inocelliidae larvae require a period ofstatic hibernation to complete their life cycle (Kovarik et al. 1991). If the final larval stage isnot exposed to a decrease in temperature, it remains alive, active, feeds and moults, butafter weeks or months, it moults into a peculiar larva with more or less pronounced pupalcharacteristics. These larvae may undergo additional moults, but eventually they perish(Aspöck et al. 2018). Interestingly,  the  I. calida individuals  reared  in  this  study  did  notundergo  low-temperature  stimulation  during  the  larval  stage,  yet  they  successfullydeveloped into healthy adults after normal pupation. This phenomenon may be attributedto factors such as abundant food, a safe feeding environment and a small sample size.In this research, I. calida was discovered in P. koraiensis logs infected by B. xylophilus andM. saltuarius. This marks the first documented occurrence of I. calida in Liaoning Provinceand as a predator of M. saltuarius. This study was conducted under artificial conditions andthe feeding range and amount of I. calida larvae under natural conditions were not yetclear.  In  our  experiments,  I. calida was  provided  with  larvae,  pupae and adults  of  M. saltuarius,  but  it  primarily  targeted the larvae for  biting.  Further  research is  needed toexplore the developmental duration, predation targets and feeding preferences of I. calidain its natural habitat.AcknowledgementsThis work was supported by Applied Basic Research Program of Liaoning Province [grantnumbers: 2023JH2/101300130]. We thank Xingyue Liu at China Agricultural University andLiangming Cao at Key Laboratory of Forest Protection of National Forestry and GrasslandAdministration, Ecology and Nature Conservation Institute, Chinese Academy of Forestry,Beijing, China for helping with the species identification and the Dahuofang experimentalforest farm for supporting this study.Funding programThe  Applied  Basic  Research  Program  of  Liaoning  Province  [grant  numbers:2023JH2/101300130]Author contributionsYu M: Methodology, Investigation, Writing—original draft; Wang J: Investigation, Writing—original  draft;  Yan  WF:  Investigation;  Kuang  SY:  Investigation;  Zheng  YN:Inocellia (Amurinocellia) calida (Raphidioptera, Inocelliidae) was first ... 7Conceptualisation, Funding acquisition, Project administration, Writing—review and editing.All authors have read and agreed to the published version of the manuscript.Conflicts of interestThe authors have declared that no competing interests exist.References• Aspöck H, Aspöck U (1973) Inocellia (Amurinocellia n. subg.) calida n. sp.—eine neueSpezies der Familie Inocelliidae (Ins., Raphidioptera) aus Ostasien. 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Inocellia (Amurinocellia) calida (Raphidioptera, Inocelliidae) was first observed as a predator of Monochamus saltuarius (Coleoptera, Cerambycidae) in China, the vector of Bursaphelenchus xylophilus (Aphelenchida, Aphelenchoididae)

Monochamus saltuarius Gebler (Coleoptera, Cerambycidae) serves as the primary carrier of Bursaphelenchus xylophilus (Steiner & Buhrer) (Aphelenchida, Aphelenchoididae) in the middle-temperate zone of China. Pine wilt disease caused by B. xylophilus leads to serious losses to pine forestry around the world. It is necessary to study the biological control of M. saltuarius to effectively prevent the further spread of B. xylophilus. To explore the insect resources that act as natural enemies of M. saltuarius, investigations were conducted on natural enemy insects by splitting Pinus koraiensis Siebold & Zucc (Pinales, Pinaceae) damaged by M. saltuarius and dissecting their trunks in Yingpan Village, Fushun County, Fushun City, Liaoning Province, China, in 2023. A larva of Inocellia (Amurinocellia) calida (H. Aspöck & U. Aspöck) (Raphidioptera, Inocelliidae) was discovered in the trunk of an infested P. koraiensis. Additionally, the feeding habits of I. calida were preliminarily examined under indoor conditions and a description of its morphological characteristics was provided. When placed in an indoor environment, the I. calida larva began pupating after a period of 21 days, during which time it consumed and attacked a total of 23 M. saltuarius larvae. Ultimately, after a pupal period of ten days, the I. calida larva emerged successfully as an adult. This discovery marks the first recorded presence of I. calida in Liaoning Province and the first documentation of I. calida in China, serving as a natural predatory enemy of M. saltuarius

Inocellia (Amurinocellia) calida (Raphidioptera, Inocelliidae) was first observed as a predator of Monochamus saltuarius (Coleoptera, Cerambycidae) in China, the vector of Bursaphelenchus xylophilus (Aphelenchida, Aphelenchoididae)

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