Skip to main content
SpringerLink
Log in

Commensal relation between Bursaphelenchus xylophilus (Nematoda: Aphelenchoididae) and Monochamus alternatus (Coleoptera: Cerambycidae) within pine trees

  • Original Research Paper
  • Published:
Applied Entomology and Zoology Aims and scope Submit manuscript

Abstract

Bursaphelenchus xylophilus (Steiner et Buhrer) Nickle causes pine wilt disease and is transmitted by Monochamus alternatus Hope adults in Japan. To determine the effects of the beetle larvae on the nematode population and the effects of the nematode population on beetle larval growth, we inoculated fresh pine bolts with various combinations of B. xylophilus, M. alternatus, and the blue-stain fungus Ophiostoma minus (Hedgc.) Syd. & P. Syd., the food of the nematodes. We also compared the content of ergosterol among the phloem, xylem, and larval frass. The nematode density was 22 or 25 times higher in frass than in phloem and the lowest in xylem, indicating positive effects of beetle larvae on the nematode population growth. Frass had twice higher ergosterol content than the phloem, indicating the fungal mycelial content was greatest in the frass. The difference in the content of fungal mycelia could explain in part the difference in B. xylophilus density between the frass and phloem. By contrast, B. xylophilus did not affect the growth and developmental rate of M. alternatus. This study showed that the relation between the beetle and nematode populations changes from mutualism to commensalism corresponding to the dispersal to reproduction stages of the nematode population.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Akbulut S, Linit MJ (1999) Flight performance of Monochamus carolinensis (Coleoptera: Cerambycidae) with respect to nematode phoresis and beetle characteristics. Environ Entomol 28:1014–1020

    Article  Google Scholar 

  • Arakawa Y, Togashi K (2002) Newly discovered transmission pathway of Bursaphelenchus xylophilus from males of the beetle Monochamus alternatus to Pinus densiflora trees via oviposition wounds. J Nematol 34:396–404

    PubMed Central  PubMed  Google Scholar 

  • Carlile MJ, Watkinson SC, Gooday GW (2001) The fungi, 2nd edn. Academic Press, New York

    Google Scholar 

  • Dowding P (1970) Colonization of freshly bared pine sapwood surfaces by staining fungi. Trans Br Mycol Soc 55:399–412

    Article  Google Scholar 

  • Edwards OR, Linit MJ (1992) Transmission of Bursaphelenchus xylophilus through oviposition wounds of Monochamus carolinensis (Coleoptera: Cerambycidae). J Nematol 24:133–139

    PubMed Central  CAS  PubMed  Google Scholar 

  • Haack RA, Slansky F (1987) Nutritionalecology of wood-feeding Coleoptera, Lepidoptera, and Hymenoptera. In: Slansky F, Rodriguez JG (eds) Nutritional ecology of insects, mites, spiders, and related invertebrates. Wiley, New York, pp 449–486

    Google Scholar 

  • Ichihara Y, Fukuda K, Suzuki K (2000) Early symptom development and histological changes associated with migration of Bursaphelenchus xylophilus in seedling tissues of Pinus thunbergii. Plant Dis 84:675–680

    Article  Google Scholar 

  • Kanzaki N, Futai K (2001) Life history of Bursaphelenchus conicaudatus (Nematoda: Apehelenchoididae) in relation to the yellow-spotted longicorn beetle, Psachothea hilaris (Coleoptera: Cerambycidae). Nematology 3:473–479

    Article  Google Scholar 

  • Kanzaki N, Futai K (2002) Life history of Rhabdontolaimus psacotheae (Diplogasterida: Diplogasteroididae) and its habitat segregation from Bursaphelenchus conicaudatus (Aphelenchida: Aphelenchoididae). Jpn J Nematol 32:60–68

    Article  Google Scholar 

  • Kaya HK (1984) Nematode parasites of bark beetles. In: Nickle WR (ed) Plant and insect nematodes. Marcel Dekker, New York, pp 727–754

    Google Scholar 

  • Kobayashi T, Sasaki K, Mamiya Y (1974) Fungi associated with Bursaphelenchus lignicolus, the pine wood nematode (I). J Jpn Soc 56:136–145 (in Japanese with English summary)

    Google Scholar 

  • Kojima K, Katagiri K (1964) On the larval instar and changes of its composition of Monochamus alternatus Hope. J Jpn Soc 46:307–310 (in Japanese with English summary)

    Google Scholar 

  • Kuroda K, Ito S (1992) Migration speed of pine wood nematodes and activities of other microbes during the development of pine-wilt disease in Pinus thunbergii. J Jpn Soc 74:383–389 (in Japanese with English summary)

    Google Scholar 

  • Maehara N, Futai K (2000) Population changes of the pinewood nematode, Bursaphelenchus xylophilus (Nematoda: Aphelenchoididae), on fungi growing in pine-branch segments. Appl Entomol Zool 35:413–417

    Article  Google Scholar 

  • Mamiya Y (1983) Pathology of the pine wilt disease caused by Bursaphelenchus xylophilus. Annu Rev Phytopathol 21:201–220

    Article  CAS  PubMed  Google Scholar 

  • Mamiya Y, Enda N (1972) Transmission of Bursaphelenchus lignicolus (Nematoda: Aphelenchoididae) by Monochamus alternatus (Coleoptera: Cerambycidae). Nematologica 18:159–162

    Article  Google Scholar 

  • Massey CL (1974) Biology and taxonomy of nematode parasites and associates of bark beetles in the United States, Agricultural Handbook 446. USDA Forestry Service, Washington

    Google Scholar 

  • Matsunaga K, Togashi K (2009) Seasonal change in susceptibility of Pinus densiflora to Bursaphelenchus xylophilus infection, determined from the number of nematodes passing through branch sections. Nematology 11:409–418

    Article  Google Scholar 

  • Ochi K (1975) Ecological studies on the Japanese pine sawyer, Monochamus alternatus Hope (Coleoptera: Cerambycidae). II. Size of the first instar larva. In: Transactions of the 86th annual meeting of the Japanese Forestry Society. pp 323–324 (in Japanese)

  • Oku H, Shiraishi T, Chikamatsu K (1989) Active defense as a mechanism of resistance in pine against pine wilt disease. Ann Phytopathol Soc Jpn 55:603–608

    Article  Google Scholar 

  • Rutherford TA, Webster JM (1987) Distribution of pine wilt disease with respect to temperature in North America, Japan, and Europe. Can J Res 17:1050–1059

    Article  Google Scholar 

  • Rühm W (1956) Die Nematoden der Ipiden. Parasitologische Schriftenreihe 6:1–435

    Google Scholar 

  • Seitz LM, Mohr HE, Burroughs R, Sauer DB (1977) Ergosterol as an indicator of fungal invasion in grains. Cereals Chem 54:1207–1217

    CAS  Google Scholar 

  • Son JA, Komatsu M, Matsushita N, Hogetsu T (2010) Migration of pine wood nematodes in the tissues of Pinus thunbergii. J Res 15:186–193

    Article  CAS  Google Scholar 

  • Sudhaus W, von Lieven AF (2003) A phylogenetic classification and catalogue of the Diplogastridae (Secernentea, Nematoda). J Nematode Morphol System 6:43–89

    Google Scholar 

  • Togashi K (1991) Different developments of overwintered larvae of Monochamus alternatus (Coleoptera: Cerambycidae) under a constant temperature. Jpn J Entomol 59:149–154

    Google Scholar 

  • Togashi K (1997) Lifetime fecundity and body size of Monochamus alternatus (Coleoptera: Cerambycidae) at a constant temperature. Jpn J Entomol 65:458–470

    Google Scholar 

  • Togashi K (2014) Effects of larval food shortage on diapause induction and adult traits in Taiwanese Monochamus alternatus alternatus. Entomol Exp Appl 151:34–42

    Article  Google Scholar 

  • Togashi K, Matsunaga K (2003) Between-isolate difference in dispersal ability of Bursaphelenchus xylophilus and the vulnerability to inhibition by Pinus densiflora. Nematology 5:559–564

    Article  Google Scholar 

  • Togashi K, Sekizuka H (1982) Influence of the pine wood nematode, Bursaphelenchus lignicolus (Nematoda: Aphelenchoididae), on longevity of its vector, Monochamus alternatus (Coleoptera: Cerambycidae). Appl Entomol Zool 17:160–165

    Google Scholar 

  • Wingfield MJ, Blanchette RA (1983) The pine-wood nematode, Bursaphelenchus xylophilus in Minnesota and Wisconsin: insect associates and transmission studies. Can J Res 13:1068–1076

    Article  Google Scholar 

  • Wingfield MJ, Blanchette RA, Nicholls TH (1984) Is the pine wood nematode an important pathogen in the United States? J Forestry 82:232–235

    Google Scholar 

  • Zhao LL, Lu M, Niu HT, Fang GF, Zhang SA, Sun JH (2013) A native fungal symbiont facilitates the prevalence and development of an invasive pathogen-native vector symbiosis. Ecology 94:2817–2826

    Article  PubMed  Google Scholar 

  • Zhao LL, Mota M, Vieira P, Butcher RA, Sun JH (2014) Interspecific communication between pinewood nematode, its insect vector, and associated microbes. Trends Parasitol 30:299–308

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful to Dr. W. Toki for providing some adults and larvae of Taiwanese M. alternatus and to staff members of University of Tokyo Tanashi Forest, University of Tokyo, for helping to transfer pine logs. We also thank Prof. Y. Yamaoka of Tsukuba University and two anonymous reviewers for the information on the dispersal of blue-stain fungi and for invaluable comments, respectively. This work was supported in part by JSPS KAKENHI grants (nos. 22380081 and 26292080). The introduction of prohibited articles was permitted under special conditions by the Minister of Agriculture, Forestry, and Fisheries, Japan (21Y1218).

Author information

Author notes

  1. Osamu Miyauchi

    Present address: Laboratory of Agricultural and Development Economics, Graduate School of Agricultural and Life Sciences, University of Tokyo, Yayoi, Bunkyo-ku, Tokyo, 113-8657, Japan

Authors and Affiliations

  1. Laboratory of Forest Zoology, Graduate School of Agricultural and Life Sciences, University of Tokyo, Yayoi, Bunkyo-ku, Tokyo, 113-8657, Japan

    Katsumi Togashi

  2. Major in Forest Life Science, Faculty of Agriculture, University of Tokyo, Yayoi, Bunkyo-ku, Tokyo, 113-8657, Japan

    Osamu Miyauchi

  3. University of Tokyo Tanashi Forest, Graduate School of Agricultural and Life Sciences, University of Tokyo, Nishi-Tokyo, Tokyo, 188-0002, Japan

    Dai Kusumoto

  4. Laboratory of Forest Botany, Graduate School of Agricultural and Life Sciences, University of Tokyo, Yayoi, Bunkyo-ku, Tokyo, 113-8657, Japan

    Norihisa Matsushita

Authors
  1. Katsumi Togashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Osamu Miyauchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dai Kusumoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Norihisa Matsushita
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Katsumi Togashi.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Togashi, K., Miyauchi, O., Kusumoto, D. et al. Commensal relation between Bursaphelenchus xylophilus (Nematoda: Aphelenchoididae) and Monochamus alternatus (Coleoptera: Cerambycidae) within pine trees. Appl Entomol Zool 51, 53–62 (2016). https://doi.org/10.1007/s13355-015-0370-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13355-015-0370-7

Keywords

Search

Navigation