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/lp/springer-journals/insecticidal-effect-of-the-entomopathogenic-nematode-heterorhabditis-l3qFBoYUAF
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- Springer Journals
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- Copyright © The Author(s) 2023
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- 10.1007/s13355-023-00820-1
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Abstract
To scout for an entomopathogenic nematode (EPN) that effectively controls the pine sawyer beetle, Monochamus alternatus Hope (Coleoptera: Cerambycidae), we screened EPNs from soil samples using M. alternatus larvae as bait. A population of the nematode obtained was named isolate SOz01, and molecularly identified as Heterorhabditis megidis Poinar, Jackson and Klein (Nematoda: Heterorhabditidae). In the inoculation test of the infective juveniles (IJs) of SOz01 onto mature larvae of M. alternatus under laboratory conditions, a mortality of 86–100% occurred when more than 20 IJs were inoculated. Even when the larvae were inoculated with only five IJs, one-third of them died. This finding suggests that H. megidis SOz01 has a strong insecticidal effect on M. alternatus. Keywords Bait trapping · Infective juvenile · Inoculation test · Molecular identification · Soil screening Introduction through fumigating damaged trees and spraying chemical insecticides onto live pine trees (Kamata 2008). On the other The pine sawyer beetle, Monochamus alternatus Hope hand, the use of the natural enemies of vector insects has (Coleoptera: Cerambycidae), is the principal vector of the long been studied (Shimazu 2008). Thus far, no practical pinewood nematode, Bursaphelenchus xylophilus (Steiner use of a biological agent has been achieved, except for the and Buhrer) Nickle (Nematoda: Aphelenchoididae), the entomopathogenic fungus Beauveria bassiana (Balsamo) causal agent of pine wilt disease (PWD), in Japan, Korea, Vuillemin (Shimazu and Higuchi 2007). and China (Kishi 1995; Shin 2008; Zhao 2008). In Japan, Entomopathogenic nematodes (EPNs) primarily com- PWD is usually controlled by killing the vector insects prise the Heterorhabditidae and Steinernematidae families (Grewal et al. 2005) and possess a symbiotic relationship with entomopathogenic bacteria of the genera Photorhabdus * Sota Ozawa and Xenorhabdus, respectively (Poinar 1979, 1990). EPNs sozawa@ffpri.affrc.go.jp undergo an infective juvenile stage (IJ) in their life cycles. Noritoshi Maehara They invade the insect host through the mouth, anus, and tra- maehara@ffpri.affrc.go.jp cheal system, and then release their symbiotic bacteria into Jun Takatsuka the hemocoels (Goodrich-Blair and Clarke 2007). The toxins junsan@ffpri.affrc.go.jp produced by the bacteria kill the insect and the propagated Takuya Aikawa nematodes emerge from the cadaver as IJs to seek a new host taikawa@ffpri.affrc.go.jp (Poinar and Thomas 1966). Katsunori Nakamura There have been several studies on the insecticidal activ- knakam@ffpri.affrc.go.jp ity of EPNs against M. alternatus (Katagiri et al. 1984; Tohoku Research Center, Forestry and Forest Products Mamiya and Shoji 1986; Mamiya 1989; Yamanaka 1993; Yu Research Institute, 92-25 Nabeyashiki, Shimo-Kuriyagawa, et al. 2016). High insecticidal rates of M. alternatus larvae Morioka, Iwate 020-0123, Japan treated with EPNs have been attained under experimental Department of Forest Entomology, Forestry and Forest conditions; however, their practical use in the field has not Products Research Institute, 1 Matsunosato, Tsukuba, been achieved. This is probably because of the insufficient Ibaraki 305-8687, Japan Vol.:(0123456789) 1 3 Applied Entomology and Zoology mobility of the nematodes to penetrate under the bark and their survival. When a larva was immobile and the body access the M. alternatus larvae living deep in the wood color turned black or red, it was regarded as dead. (Phan 2008). Furthermore, the EPNs employed in these stud- Each dead larva was washed with distilled water (DW) ies were originally used to control other insect species. In and individually placed on a 55-mm filter paper (ADVAN- bait trapping to screen EPNs, Galleria mellonella L. (Lepi- TEC, No. 1) in a 6-cm plastic Petri dish. The Petri dish was doptera: Pyralidae) has been widely used as the bait insect wrapped with ParafilmM® (Bemis Flexible Packaging) to (Bedding and Akhurst 1975), whereas there are attempts to avoid drying and incubated in the dark at 25 °C. Thereaf- use the insects to be controlled as bait (Kushida et al. 1986, ter, we checked the larval body color and the presence of 1987; Mamiya 1988, 1989). The screening of EPNs using nematodes inside the larval body once every 2–3 days. A M. alternatus as bait may yield an EPN that has a strong larva that showed a reddish body color and had nematodes insecticidal ee ff ct on M. alternatus under natural conditions. inside its body was transferred to the White trap (White In this study, we screened EPNs from soil using M. alter- 1927) to collect the IJs of the EPN according to the fol- natus larvae as bait. The EPN obtained was molecularly lowing procedure: a lid of 6-cm plastic Petri dish (8.8 mm identified and its insecticidal effect against M. alternatus high) was placed in the center of an unsterilized 9-cm glass larvae was evaluated under laboratory conditions. Petri dish (21 mm deep); three pieces of 55-mm filter paper were placed so that the outermost edges were soaked in DW poured in the 9-cm Petri dish; the dead larva was placed on Materials and methods the filter paper; the nematodes that emerged from the larval body were trapped in the water. Insects used The EPN obtained was inoculated on M. alternatus lar- vae. We placed a larva on DW-moistened filter paper in a The insects used were the mature M. alternatus larvae reared 6-cm plastic Petri dish and applied a 0.5-mL suspension con- in our laboratory using the artificial diet reported by Mae- taining 25 IJs of the EPN directly onto the larval body. Once hara et al. (2018), which originated from the insects obtained the larva died, it was transferred to the White trap to collect in Oshu City, Iwate Prefecture, Japan. Mature larvae were IJs propagated in the dead larva. The culture population of kept at 10 °C in the dark until used. the EPN was maintained by repeating this procedure. Screening of EPNs from soil Molecular identification of the EPN Based on the Galleria baiting method by Bedding and The genomic DNA of the EPN was extracted with extraction Akhurst (1975), we conducted a screening of EPNs from buffer supplied with the B. xylophilus Detection Kit (Nippon the soil using M. alternatus larvae as bait. Soil samples were Gene Co., Ltd.). collected from four forest sites in Iwate and Miyagi Prefec- We used primers no. 93 and no. 94 for PCR amplifica- tures, Japan (Table 1). We took 500–700 mL of soil, exclud- tion of ITS rDNA; this primer pair was designed by Stock ing leaf litter, from the forest floor at a depth of 20–30 cm, et al. (2001) and was used to determine the phylogenetic and packed it in zippered plastic bags (220 × 170 mm). The relationships of Heterorhabditis nematodes (Maneesakorn following day, approximately 350 mL of soil was transferred et al. 2011). PCR amplification was performed according to into a plastic cup (φ130 × 60 mm high) and two M. alterna- the protocol for GoTaq® G2 Hot Start Green Master Mix tus larvae were placed on the soil surface. The cup was then 2X (Promega), where the primer annealing temperature was covered with a lid and placed under dark conditions at 25 °C. 47.8 °C. The singly amplie fi d PCR product of approximately The larvae were observed daily for 27–37 days to monitor 800 bp was purified by the QIAquick PCR Purification Kit (QIAGEN). The purified sample was sequenced with ABI Table 1 Outline of the locations of soil sampling Locality Site code Latitude and longitude Dominant tree species No. of soil sam- Soil code Sampling date ples collected Morioka, Iwate a 39º 49′ 08.5" N/148º 08′ 06.7" E Pinus densiflora 1 a-1 23 May 2018 Hanamaki, Iwate b 39º 29′ 25.4" N/141º 11′ 20.9" E Pinus densiflora 3 b-1, b-2, b-3 14 June 2018 Oshu, Iwate c 39º 14′ 50.7" N/141º 08′ 04.3" E Pinus densiflora 2 c-1, c-2 23 May 2018 Ohira, Miyagi d 38º 28′ 49.5" N/140º 53′ 26.6" E Pinus densiflora 3 d-1, d-2, d-3 27 June 2018 38º 28′ 50.7" N/140º 53′ 28.8" E Cryptomeria japonica 1 d-4 27 June 2018 1 3 Applied Entomology and Zoology Fig. 1 Phylogenetic tree of Het- erorhabditis megidis and closely related species to H. megidis using sequences containing ITS-1, ITS-2, and the 5.8S ribosomal RNA gene. The phy- logenetic tree was constructed by the maximum likelihood method using 59 sequences. The final data set included 386 positions. The numbers at each branch represent the bootstrap probabilities of the branch points. The species name and the accession number of each Heterorhabditis nematode are indicated at the terminal of each branch. H. zealandica (EF530041) was set as an out- group in the phylogenetic tree. For H. megidis, the name of the country of origin was given if available; and designated “N/A” if the country was unknown. The arrow shows the nematode species obtained in this study (SOz01) PRISM® BigDye® Terminator v3.1 Cycle Sequencing Kits The ClustalW Multiple alignment using BioEdit (Applied Biosystems) using the ABI 3730xl Analyzer. v.7.0.5.3 was employed to compare sequences (Thomp- The sequence obtained was compared for homology using son et al. 1994; Hall 1999). A phylogenetic tree was con- the NCBI nucleotide BLAST. Subsequently, we conducted structed from the maximum likelihood method and the a phylogenetic analysis using the sequences of H. megidis Kimura 2-Parameter Model (Kimura 1980) using Molecu- Poinar, Jackson, and Klein, including the one obtained in lar Evolutionary Genetics Analysis v.6.0 (MEGA6) soft- this study and five closely related species (Fig. 1) obtained ware (Tamura et al. 2013). The bootstrap value was set at from the NCBI nucleotide collection database. 1000. 1 3 Applied Entomology and Zoology Insecticidal effect of the EPN The IJs of the EPN for the inoculation test were taken from the culture population. The IJs were washed three times with DW and kept for 14 days at 5 °C before the inoculation test according to the manual of EPNs by Yoshiga (2014). The inoculation test was repeated three times. The IJs used in the trials were each prepared whenever the tests were done. We set five levels of inoculum-density (i.e., number of IJs inoculated per M. alternatus larva) treatments to test the insecticidal effect: 320, 80, 20, 5, and 0 IJs (control). The M. alternatus larvae used in the test were weighed the day before EPN inoculation, and divided into five treatment groups in a manner that minimized the body weight bias between the groups (Online Resource 1). The larvae were washed with DW, immersed in 70% ethanol for 5 s, and washed with sterilized distilled water (SDW) before they were individually placed in a 6-cm plastic Petri dish with 55-mm filter paper moistened with SDW. An EPN suspen- sion containing 320, 80, 20, 5, or 0 IJs in 500 µL of SDW was dropped directly onto the insect’s body surface. A Pipetman (P-200, GILSON) attached to a transparent glass Pasteur pipette at the tip was used, making the inoculum visible and ensuring the correct number of nematodes was inoculated. The Petri dishes were wrapped with ParafilmM® and incubated in the dark at 25 °C. The larvae were observed every 24 h to check their survival. A larva was regarded as Fig. 2 Survivorship of the Monochamus alternatus larvae in the dead when it stopped moving and its body color turned red inoculation test of Heterorhabditis megidis SOz01. The upper, mid- (including partial discoloration) or black. The observation dle, and lower graphs correspond to the first, second, and third tri- was terminated when all of the larvae either died or pupated als, respectively. Different symbols indicate different inoculum-den- sity treatments (i.e., the number of nematodes inoculated per insect (Fig. 2). larva): white circles indicate zero nematodes (control), black squares Dead larva was washed with SDW and transferred to a indicate five nematodes, black triangles indicate 20 nematodes, white different 6-cm plastic Petri dish with SDW-moistened filter inverted triangles indicate 80 nematodes, and black diamonds indi- paper. The inside of the original Petri dish and both sides cate 320 nematodes per larva of the filter paper removed from the Petri dish were washed with DW. The number of nematodes detected in the wash- ing water was the lowest estimated number of IJs that did Statistical analysis not invade the larva. The dead larva was dissected within 3–4 days after expiring, and the developmental stages of The fresh weight of M. alternatus larvae used in the inocu- the EPNs (i.e., infective juvenile, fourth-stage juvenile, lation test was compared by one-way ANOVA among the hermaphrodite adult, and next-generation small juvenile) insect groups of the five different densities of inoculum treat- detected in the larval body were determined and counted. ments. We used the Kruskal-Wallis test to compare the per- For larvae in which no nematode was found by dissection, centage of EPNs detected in the dead M. alternatus larvae to we determined the cause of death based on the body color the total number of inoculated nematodes. All analyses were and tissue conditions of the cadavers. It is known that an performed by R statistical software (v.3.6.1). insect infected with H. megidis shows a unique red colora- tion (Poinar et al. 1987; Yoshiga 2014) and a dense muci- laginous appearance of its disintegrated tissues, referred to Results as “gummy consistency” by Poinar (1979). Screening of EPNs from soil A total of 20 living larvae of M. alternatus were placed on 10 soil samples (Table 1), and 16 larvae died. Among 1 3 Applied Entomology and Zoology them, one dead larva placed on soil sample b-3 taken in a compared with the treatments with 320 and 80 IJs. The over- forest stand of Japanese red pine (Pinus densiflora Sieb. all mortality was 86.7% (Table 2). In the treatment with five and Zucc.) turned its body color red, and nematodes were IJs, 5 out of 15 larvae tested died (Table 2, Fig. 2). observed moving inside the body. The nematodes derived All of the dead M. alternatus larvae in the inoculation from this larva were inoculated onto living M. alternatus test showed systemic red body color, except for one larva larvae, which were consequently infected with the nema- inoculated with 320 IJs in the second trial, which showed todes and died. Therefore, the nematode was confirmed partial black immediately after its death and then turned to to be an EPN. We named the nematode isolate obtained partial red. “SOz01”. No EPN was detected in the other 15 dead larvae We dissected a total of 47 larvae that died in the inocu- during the screening period. lation test (Table 2). They all displayed the “gummy con- sistency” of the body tissue (Poinar 1979) characteristic of Molecular identification of the EPN insects killed by EPNs. In 44 among 47 larvae dissected, we detected IJs of H. megidis and fourth-stage juveniles and/or The nucleotide sequence of 793 bp ITS rDNA for our iso- adults that had developed from the inoculated IJs (Online late SOz01 was deposited in the NCBI GenBank (http:// Resource 2). No male adults were found in the detected www . ncbi. nlm. nih. gov/ genba nk/) with accession number nematodes, and the fourth-stage juveniles did not show mor- MZ675644. A BLAST search showed that the ITS rDNA phological characteristics corresponding to the male spicule. sequence of SOz01 had a 100% homology to H. megidis Heterorhabditis megidis has been reported to develop into AB698759. hermaphrodites from IJs (Poinar et al. 1987). Therefore, we The phylogenetic tree indicated a species-specific group- considered the adult nematodes detected in the dead larvae ing (Fig. 1). SOz01 was located in the branch formed by the as hermaphrodites. Additionally, we found small juveniles, Korean samples in the group of H. megidis. Thus, we clas- which were clearly distinguishable from IJs (Table 2). sified SOz01 into H. megidis. The total number of the IJs, fourth-stage juveniles, and hermaphrodite adults detected in a dead larva was regarded Insecticidal effect of the EPN as the estimated minimum number of nematodes that suc- cessfully invaded the larva, because some of the invading In the treatment where 320 IJs were inoculated, all larvae IJs may have died and disappeared before dissection. The died within 2–5 days after inoculation (Fig. 2). The overall number of invading nematodes increased with the number of trend of larval mortality in the treatment with 80 IJs was inoculated nematodes (Table 2), although only 9–17% of the similar to that with 320 IJs (93.3%, Table 2). In the treatment inoculated nematodes invaded the larvae. There was no sig- with 20 IJs, the occurrence of larval mortality was delayed nificant difference in the percentage of invading nematodes (in the second trial) or retarded (in the first and third trials) among the inoculum-density treatments with 320, 80, 20, Table 2 Mortality of Monochamus alternatus larvae after inoculation with Heterorhabditis megidis SOz01 and the nematodes detected from the insect body or the inner surface of the container Treatment (no. of No. of No. of Mean days No. of nematodes detected from the No. of nematodes % Invading inoculated nema- insects dead until death inside of the dead insect body detected from nematodes to todes) tested insects (range) the outside of the the inoculated Invading nema- Juveniles of the a b insect body nematodes todes (infective next generation (mean ± SD) juveniles + fourth- (mean ± SD) stage juve- niles + hermaph- rodite adults) (mean ± SD) 320 15 15 3.2 (2–5) 30.3 ± 14.2 24.4 ± 80.9 134.9 ± 37.8 9% 80 15 14 3.2 (2–4) 8.2 ± 4.9 13.3 ± 39.3 26.8 ± 7.8 10% 20 15 13 5.2 (3–12) 3.3 ± 2.2 0.1 ± 0.3 5.8 ± 2.8 17% 5 15 5 5.2 (3–9) 0.8 ± 0.8 0 0.8 ± 1.3 16% 0 (Control) 15 0 – – – – – The sum of the numbers of nematodes recovered from the surface of the insect body and the inside of the container used in the test was calcu- lated b 2 There was no significant difference in the percentage of invading nematodes among the treatments (Kruskal-Wallis test: χ = 3.85, df = 3, p = 0.28) 1 3 Applied Entomology and Zoology and 5 IJs (χ = 3.85, df = 3, p = 0.28). The maximum number small number of IJs invade an insect. In fact, Yu et al. (2016) of invading nematodes detected in the dead larvae was 43 showed that none of the IJs emerged from M. alternatus even when the larvae were inoculated with 320 IJs (Online larvae inoculated with five IJs of S. carpocapsae, whereas Resource 2). In the treatment with five IJs, we detected a mean number of 60,000 IJs was obtained from the larvae one–two invading nematodes in three out of five dissected inoculated with 80 IJs. In the case of H. bacteriophora, the larvae (Online Resource 2). In a case among them (Online number of IJs obtained from the dead larvae of the rosaceae Resource 2: Code 5 IJs-21 in the second trial), we found longhorned beetle, Osphranteria coerulescens, inoculated one nematode invading the larval body and three outside the with 5 and 25 IJs was four-to-seven times greater than that insect body (insect body surface + inside of the Petri dish), when S. carpocapsae was inoculated (Sharifi et al. 2014). In indicating that the number of invading nematode was two the case of SOz01, we observed that more than 40,000 IJs at most. emerged from M. alternatus larvae inoculated with five IJs of H. megidis SOz01 (unpublished data). In conclusion, SOz01 has two advantages in control- Discussion ling the larvae of M. alternatus, i.e., the strong insecticidal effect on them and the high reproduction potential based on Heterorhabditis megidis SOz01 had a potent insecticidal a hermaphrodite. effect on M. alternatus larvae. Inoculation with more than Supplementary Information The online version contains supplemen- 20 IJs resulted in 86–100% larval mortality (Table 2, Fig. 2). tary material available at https://doi. or g/10. 1007/ s13355- 023- 00820-1 . Although there were several reports on the insecticidal effect of S. carpocapsae Weiser against M. alternatus, Yu et al.’s Acknowledgements We sincerely thank Ms. N. Kawamura, Tohoku Research Center, FFPRI, for her assistance with the laboratory exper- (2016) report was the only one that was comparable with the iments and insect rearing. This work was supported in part by the present study in terms of the level of the inoculum densities Grants-in-Aid for Scientific Research (B) (No. JP20H03038) from the (i.e., 5–80 IJs). They demonstrated 80% and 40% insect mor- Japan Society for the Promotion of Science. tality by inoculating 20 and 5 IJs, respectively, and SOz01 Data availability Data are available up on request with the correspond- showed almost the equivalent insecticidal performance. Fur- ing author. thermore, SOz01 caused mortality in M. alternatus larvae even when a small number (i.e., five) of IJs were inoculated Open Access This article is licensed under a Creative Commons Attri- bution 4.0 International License, which permits use, sharing, adapta- (Table 2, Fig. 2). We recovered four nematodes from one of tion, distribution and reproduction in any medium or format, as long the dead M. alternatus larvae inoculated with five IJs: one as you give appropriate credit to the original author(s) and the source, successfully invaded the larval body, and three were found provide a link to the Creative Commons licence, and indicate if changes on the larval body surface and inside the Petri dish (Online were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated Resource 2: Code 5 IJs-21). Although we did not find the otherwise in a credit line to the material. If material is not included in remaining one IJ of the five inoculated nematodes, we con- the article's Creative Commons licence and your intended use is not cluded that one or possibly two IJs of SOz01 could cause permitted by statutory regulation or exceeds the permitted use, you will larval mortality. need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://cr eativ ecommons. or g/licen ses/ b y/4.0/ . The detection of the various stages of nematodes (i.e., fourth-stage juveniles, hermaphrodites, and next-generation small juveniles, as well as the inoculated IJs) indicates that the inoculated IJs could propagate in the insect body within References 1 week or so, as most of the host larvae died within 3–4 days after inoculation (Online Resource 2) and they were dis- Bedding RA, Akhurst RJ (1975) A simple technique for the detec- tion of insect paristic rhabditid nematodes in soil. Nematologica sected within 3–4 days after larval death. No nematodes 21:109–110. https:// doi. org/ 10. 1163/ 18752 9275X 00419 were detected in three dead M. alternatus larvae that were Goodrich-Blair H, Clarke DJ (2007) Mutualism and pathogenesis in inoculated with 20 or 5 IJs and showed the symptom of H. Xenorhabdus and Photorhabdus: two roads to the same destina- megidis infection. The inoculated IJs would have killed the tion. Mol Microbiol 64:260–268. https:// doi. org/ 10. 1111/j. 1365- 2958. 2007. 05671.x larvae by their symbiotic bacteria but failed to develop in the Grewal PS, Ehlers R-U, Shapiro-Ilan DI (2005) Nematodes as biocon- larval body, and hence could not be detected. trol agents. CABI Publishing, Wallingford Heterorhabditis megidis is a hermaphrodite (Strauch Hall TA (1999) BioEdit: a user-friendly biological sequence alignment et al. 1994; Nguyen and Smart 1998), which can propa- editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98 gate through self-fertilization. This may be advantageous Kamata N (2008) Integrated pest management of pine wilt disease in as a biocontrol agent. For example, S. carpocapsae, as an Japan: tactics and strategies. In: Zhao BG, Futai K, Sutherland JR, amphimixis, needs both sexes to propagate and may not be Takeuchi Y (eds) Pine wilt disease. Springer, Tokyo, pp 304–322 able to reproduce because of a bias in the sex ratio when a 1 3 Applied Entomology and Zoology Katagiri K, Mamiya Y, Shimazu M, Tamura H, Kusida T (1984) A Eubacteriales) in the development of the nematode, DD-136 spray application of Steinernema feltiae on pine logs infected (Neoaplectana sp. Steinernematidae). Parasitology 56:385–390. with the pine sawyer, Monochamus alternatus, and its mortal-https:// doi. org/ 10. 1017/ S0031 18200 00709 80 ity induced by the nematode. Trans Jpn For Soc 95:479–480 (in Sharifi S, Karimi J, Hosseini M, Rezapanah M (2014) Efficacy of two Japanese) entomopathogenic nematode species as potential biocontrol agents Kimura M (1980) A simple method for estimating evolutionary rates against the rosaceae longhorned beetle, Osphranteria coerule- of base substitutions through comparative studies of nucleotide scens, under laboratory conditions. Nematology 16:729–737. sequences. J Mol Evol 16:111–120. https:// doi. or g/ 10. 1007/ https:// doi. org/ 10. 1163/ 15685 411- 00002 802 BF017 31581 Shin SC (2008) Pine wilt disease in Korea. In: Zhao BG, Futai K, Kishi Y (1995) The pine wood nematode and the Japanese pine sawyer. Sutherland JR, Takeuchi Y (eds) Pine wilt disease. Springer, Thomas Company Limited, Tokyo Tokyo, pp 26–32 Kushida T, Mamiya Y, Mitsuhashi J (1986) Isolation of an insect para- Shimazu M (2008) Biological control of the Japanese pine sawyer bee- sitic nematode, Neoaplectana sp., and its ability to kill the host. tle, Monochamus alternatus. In: Zhao BG, Futai K, Sutherland JR, Trans Kanto Br Jpn For Soc 37:163–164 (in Japanese) Takeuchi Y (eds) Pine wilt disease. Springer, Tokyo, pp 351–370 Kushida T, Mamiya Y, Mitsuhashi J (1987) Pathogenicity of newly Shimazu M, Higuchi T (2007) “BIOLISA MADARA”, a microbial detected Steinernema sp. (Nematoda) to scarabaeid larvae inju- insecticide for control of Monochamus alternatus adults. For Pests rious to tree seedlings. Jpn J Appl Entomol Zool 31:144–149. 56:233–239 (in Japanese) https:// doi. org/ 10. 1303/ jjaez. 31. 144 (in Japanese with English Stock SP, Campbell JF, Nadler SA (2001) Phylogeny of Steinernema abstract) Travassos, 1927 (Cephalobina: Steinernematidae) inferred from Maehara N, Kanzaki N, Aikawa T, Nakamura K (2018) Effect of Mono- ribosomal DNA sequences and morphological characters. J chamus grandis (Coleoptera: Cerambycidae) on phoretic stage Parasitol 87:877–889. https:// doi. org/ 10. 1645/ 0022- 3395(2001) formation of Bursaphelenchus xylophilus (Nematoda: Aphelen-087[0877: POSTCS] 2.0. CO;2 choididae) and the transfer of nematodes to the beetle. Nematol- Strauch O, Stoessel S, Ehlers R-U (1994) Culture conditions define ogy 20:43–48. https:// doi. org/ 10. 1163/ 15685 411- 00003 123 automictic or amphimictic reproduction in entomopathogenic Mamiya Y (1988) Steinernema kushidai n. sp. (Nematoda: Steinerne- rhabditid nematodes of the genus Heterorhabditis. Fundam Appl matidae) associated with scarabaeid beetle larvae from Shizuoka, Nematol 17:575–582 Japan. Appl Entomol Zool 23:313–320. https://do i. org/10 . 1303/ Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: aez. 23. 313 molecular evolutionary genetics analysis version 6.0. Mol Biol Mamiya Y (1989) Comparison of the infectivity of Steinernema kushi- Evol 30:2725–2729. https:// doi. org/ 10. 1093/ molbev/ mst197 dai (Nematode: Steinernematidae) and other steinernematid and Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improv- heterohabditid nematodes for three different insects. Appl Ento - ing the sensitivity of progressive multiple sequence alignment mol Zool 24:302–308. https:// doi. org/ 10. 1303/ aez. 24. 302 through sequence weighting, position-specific gap penalties and Mamiya Y, Shoji T (1986) Trials for application of Steinernema feltiae weight matrix choice. Nucleic Acids Res 22:4673–4680. https:// on pine logs infested with the pine sawyer, Monochamus alter-doi. org/ 10. 1093/ nar/ 22. 22. 4673 natus. Trans Kanto Br Jpn For Soc 38:179–180 (in Japanese) White GF (1927) A method for obtaining infective nematode larvae Maneesakorn P, An R, Daneshvar H, Taylor K, Bai X, Adams BJ, Gre- from cultures. Science 66:302–303. https://doi. or g/10. 1126/ scien wal PS, Chandrapatya A (2011) Phylogenetic and cophylogenetic ce. 66. 1709. 302.b relationships of entomopathogenic nematodes (Heterorhabditis: Yamanaka S (1993) Field control of the Japanese pine sawyer, Mono- Rhabditida) and their symbiotic bacteria (Photorhabdus: Entero- chamus alternatus (Coleoptera: Cerambycidae) larvae by Stein- bacteriaceae). Mol Phylogenet Evol 59:271–280. https:// doi. org/ ernema carpocapsae (Nematoda: Rhabditida). Jpn J Nematol 10. 1016/j. ympev. 2011. 02. 012 23:71–78. https:// doi. org/ 10. 3725/ jjn19 93. 23.2_ 71 Nguyen KB, Smart GC Jr (1998) Morphology of the life stages of three Yoshiga T (2014) Laboratory methods for testing the insecticidal activ- Heterorhabiditis spp. from the infective juvenile to the hermaph- ity of entomopathogenic nematodes. In: Mizukubo T, Futai K rodite. Soil Crop Sci Soc Florida Proc 57:101–107 (eds) Nematological experimentation. Kyoto University Press, Phan LK (2008) Potential of entomopathogenic nematodes for control- Kyoto, pp 265–267 (in Japanese) ling the Japanese pine sawyer, Monochamus alternatus. In: Zhao Yu HB, Jung YH, Lee SM, Choo HY, Lee DW (2016) Biological con- BG, Futai K, Sutherland JR, Takeuchi Y (eds) Pine wilt disease. trol of Japanese pine sawyer, Monochamus alternatus (Coleop- Springer, Tokyo, pp 371–379 tera: Cerambycidae) using Korean entomopathogenic nematode Poinar GO Jr (1979) Nematodes for biological control of insects. CRC isolates. Korean J Pestic Sci 20:361–368. https://doi. or g/10. 7585/ Press, Boca Raton. https:// doi. org/ 10. 1201/ 97813 51074 957kjps. 2016. 20.4. 361 (in Korean with English abstract) Poinar GO Jr (1990) Taxonomy and biology of Steinernematidae and Zhao BG (2008) Pine wilt disease in China. In: Zhao BG, Futai K, Heterorhabditidae. In: Gaugler R, Kaya HK (eds) Entomopatho- Sutherland JR, Takeuchi Y (eds) Pine wilt disease. Springer, genic nematodes in biological control. CRC Press, Boca Raton, Tokyo, pp 18–25 pp 23–61 Poinar GO Jr, Jackson T, Klein M (1987) Heterorhabditis megidis sp. Publisher's Note Springer Nature remains neutral with regard to n. (Heterorhabditidae: Rhabditida), parasitic in the Japanese bee- jurisdictional claims in published maps and institutional affiliations. tle, Popillia japonica (Scarabaeidae: Coleoptera), in Ohio. Proc Helminthol Soc Wash 54:53–59 Poinar GO Jr, Thomas GM (1966) Significance of Achromobac- ter nematophilus Poinar and Thomas (Achromobacteraceae: 1 3
Journal
Applied Entomology and Zoology – Springer Journals
Published: May 1, 2023
Keywords: Bait trapping; Infective juvenile; Inoculation test; Molecular identification; Soil screening