Skip to main content
Log in

Occurrence of pathogens and nematodes in forest beetles from Curculionidae and Attelabidae in Bulgaria

  • Original Article
  • Published:
Biologia Aims and scope Submit manuscript

Abstract

Beetles from Curculionidae and Attelabidae collected from 14 localities (mainly in coniferous stands) in Bulgaria were investigated for the presence of pathogens and nematodes. A microsporidium belonging to genus Nosema in the fat body of Pityogenes chalcographus (prevalence: 0.9%) and the fungus Beauveria bassiana in the oak-leaf roller Attelabus nitens (prevalence: 62%) were detected for the first time. Morphological data and characteristics of Nosema sp. spores and conidia of B. bassiana are presented. Nematode species (Cryptaphelenchus diversispicularis, Parasitorhabditis subelongati and Parasitylenchus dispar), and specimens belonging to other ten nematode genera were found (Bovianema, Bursaphelenchus, Cryptaphelenchus, Neoparasitylenchus, Parasitylenchus, Parasitaphelenchus, Panagrolaimus, Parasitorhabditis, Prothallonema and Sulphuretylenchus). Their prevalences varied from 17.4% to 90%. Nine of the host beetles (Dryocoetes autographus, Ips sexdentatus, I. acuminatus, Orthotomicus laricis, O. erosus, Pityogenes quadridens, P. conjunctus, Hylurgus ligniperda and Taphrorychus villifrons) are reported as vectors of Bursaphelenchus sp.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Ashraf M, Berryman AA (1970) Biology of Sulphuretylenchus elongatus (Nematoda: Sphaerulariidae) and its effect on its host, Scolytus ventralis (Coleoptera Scolytidae). Can Entomol 102:197–213

    Article  Google Scholar 

  • Becnel JJ (2012) Complementary techniques: preparations of entomopathogens and diseased specimens for more detailed study using microscopy. In: Lacey LA (ed) Manual of techniques in invertebrate pathology. Elsevier, San Diego, pp 451–470. https://doi.org/10.1016/B978-0-12-386899-2.00015-4

    Chapter  Google Scholar 

  • Bovien P (1937) Some types of association between nematodes and insects. Vid Meddel Dansk Naturh Forening Kobenhavn 101:1–114

    Google Scholar 

  • Braasch H (2001) Bursaphelenchus species in conifers in Europe: distribution and morphological relationship between species. EPPO Bulletin 31:127–142

    Article  Google Scholar 

  • Burjanadze M, Goginashvili N (2009) Occurrence of pathogens and nematodes in the spruce bark beetles, Ips typographus (Col., Scolytidae) in Borjomi Gorge. Bull Georg Natl Acad Sci 3(1):145–150

    Google Scholar 

  • Draganova S, Takov D, Doychev D (2007) Bioassays with isolates of Beauveria bassiana (Bals.) Vuill. And Paecilomyces farinosus (Holm.) Brown & Smith against Ips sexdentatus Boerner and Ips acuminatus Gyll. (Coleoptera: Scolytidae). Plant Sci 44(1):24–28

    Google Scholar 

  • Draganova S, Takov D, Doychev D (2010) Naturally occurred entomopathogenic fungi on three bark beetle species (Coleoptera: Curculionidae) in Bulgaria. Pesticides & Phytomedicine 25(1):59–63

    Article  Google Scholar 

  • Filipjev IN, Schuurmans Stekhoven JN (1941) A manual of agricultural Helmintology. E. J. Brill, Leiden

    Google Scholar 

  • Fuchs AG (1915) Die Naturgeschichte der Nematoden und einiger anderer Parasiten. 1. Des Ips typographus L. 2. Des Hylobius abietis L. Zoologishe Jahrbucher, Abteilung für Systematik, Oekologie und Geographie der Tiere 38:109–222

    Google Scholar 

  • Fuchs AG (1930) Neue an Borken und Rüsselkafer gebundene Nematoden, halbparasitische und Wohnungseinmieter. Freilebende Nematoden aus Moos und Walderde in Borken und Rüsselkäfergängen. Zool Jahrb, Jena. Abt Syst 59:505–646

    Google Scholar 

  • Goettel MS, Poprawski TJ, Vandenberg JD, Li Z, Roberts DW (1990) Safety to nontarget invertebrates of fungal biocontrol agents. In: Laird M, Lacey LA, Davidson EW (eds) Safety of microbial insecticides. CRC Press, Boca Raton, pp 209–231

    Google Scholar 

  • Grucmanová Š, Holuša J (2013) Nematodes associated with bark beetles, with focus on the genus Ips (Coleoptera: Scolytinae) in Central Europe. Acta zool bulg 65(4):547–556

    Google Scholar 

  • Grucmanová Š, Holuša J, Nermuť J (2014) Nematodes associated with the double-spined bark beetle Ips duplicatus (Coleoptera: Curculionidae) in Central Europe. J Appl Entomol 138(10):723–732. https://doi.org/10.1111/jen.12142

    Article  Google Scholar 

  • Grucmanová Š, Holuša J, Čermák V, Nermuť J (2016) Nematodes associated with Ips cembrae (Coleoptera: Curculionidae): comparison of generations, sexes and sampling methods. J Appl Entomol 140(5):395–403. https://doi.org/10.1111/jen.12269

    Article  Google Scholar 

  • Händel U (2001) Untersuchungen zum Gegenspielerkomplex assoziiert lebender Fichtenborkenkäfer (Col., Scolytidae) aus naturnahen und sekundären Fichtenbeständen unter besonderer Berücksichtigung der Pathogene. Dissertation, BOKU-University, Vienna

  • Händel U, Wegensteiner R (2003) Zum Auftreten von Borkenkäfern (Col., Scolytidae) an Fichten-Fangbäumen (Picea abies (L.) Karst.) aus sekundären und naturnahen Beständen in Österreich. Centralblatt für das gesamte Forstwesen 120(2):117–136

    Google Scholar 

  • Holuša J, Lukášová K, Žižka Z, Händel U, Haidler B, Wegensteiner R (2016) Occurrence of Microsporidium sp. and other pathogens in Ips amitinus (Coleoptera: Curculionidae). Acta Parasitol 61(3):621–628. https://doi.org/10.1515/ap-2016-0083

    Article  PubMed  Google Scholar 

  • Holuša J, Lukášová K, Hubáčková J, Knížek M, Wegensteiner R (2017) Pathogens and nematodes associated to three bark beetle species of the genus Orthotomicus (Coleoptera Curculionidae) in central-South Europe. Bulletin of Insectology 70(2):291–297

    Google Scholar 

  • Humber R (1997) Fungi: identification. In: Lacey LA (ed) Manual of techniques in insect pathology. Academic Press, San Diego, pp 153–163. https://doi.org/10.1016/B978-0-12-432555-5.X5000-3

    Chapter  Google Scholar 

  • Korentchenko EA (1992) Panagrolaimus orthotomici sp. n. (Cephalobina), a nematode of bark beetles of the genus Panagrolaimus in North-Eastern Asia. Parazitologiya 26:530–534 [In Russian, English summary]

  • Kulinich OA, Orlinskii PD (1998) Distribution of conifer beetles (Scolytidae, Curculionidae, Cerambycidae) and wood nematodes (Bursaphelenchus spp.) in European and Asian Russia. OEPP/EPPO Bulletin 28:39–52

  • Landa Z, Hornak P, Bursova E (2001) Entomopatogenni houby asociované s lýkožroutem smrkovým Ips typographus L. (Coleoptera, Scolytidae) v oblasti NP a CHKO Šumava. Aktuality Šumavského Výzkumu 2-4:124–128

    Google Scholar 

  • Laumond C, Carle P (1971) Nématodes associés et parasites de Blastophagus destruens Woll. [Col. Scolytidae]. Entomophaga 16(1):51–66

    Article  Google Scholar 

  • Lieutier F (1981) Influence des nématodes parasites sur l’essaimage du scolytide Ips sexdentatus (Boern.) Action régulatrice du froid. Acta Oecol Oecolo Appl 2(4):357–368

  • Lieutier F (1982) Les variations pondérales du tissue adipeux et des avaires, et les variations de longueur des ovocytes, chez Ips sexdentatus Boern (Coleoptera: Scolytidae); relations avec le parasitisme par les nématodes. Ann Parasitol Hum Comp 57(4):407–418

    Article  CAS  PubMed  Google Scholar 

  • Lieutier F (1984) Observations histologiques sur les capsules induites par Contortylenchus diplogaster v. Lins. (Nematoda: Allantonematidae) dans le tissu adipeux d’Ips sexdentatus Boern. (Coleoptera: Scolytidae). Ann Parasitol Hum Comp 59(3):245–251

    Article  CAS  PubMed  Google Scholar 

  • Linit MJ (1988) Nematode-vector relationships in the pine wilt disease system. J Nematol 20(2):227–235

  • Linstow OFB (1890) Über Allantonema und Diplogaster. Centralbl Bakteriol 8(16):489–493

    Google Scholar 

  • Lipa JJ (1968) Stempellia scolyti Weiser comb. nov. and Nosema scolyti sp. n. microsporidian parasites of four species of Scolytus (Coleoptera). Acta Protozool 6:69–84

    Google Scholar 

  • Markova G (1992) Beauveria bassiana (Bals.) Vuillemin as a pathogen of ash weevil, Stereonychus fraxini Deg. (Col., Curculionidae), in Bulgaria. J Appl Entomol 114:275–279

    Article  Google Scholar 

  • Massey CL (1964) The nematode parasites and associates of the fir engraver beetle, Scolytus ventralis LeConte, in New Mexico. J Insect Physiol 6(2):133–155

    Google Scholar 

  • Michalková V, Krascsenitsová E, Kozánek M (2012) On the pathogens of the spruce bark beetle Ips typographus (Coleoptera: Scolytinae) in the Western Carpathians. Biologia 67(1):217–221. https://doi.org/10.2478/s11756-011-0154-7

    Article  Google Scholar 

  • Nedelchev S, Takov D, Pilarska D (2008) Parasitic and associated nematodes of bark beetles in Bulgaria. Acta zool bulg, Suppl 2:83–91

    Google Scholar 

  • Nedelchev S, Takov D, Pilarska D (2011) Prothallonema tomici n. sp. (Tylenchida: Sphaerulariidae) parasitizing Tomicus piniperda (Coleoptera: Curculionidae: Scolytinae) in Bulgaria. Nematology 13(6):741–746

    Article  Google Scholar 

  • Nickle WR (1963) Observation on the effect of nematodes on Ips confusus (LeConte) and other bark beetles. J Insect Pathol 5:386–389

    Google Scholar 

  • Nickle WR (1971) Behavior of the shothole borer, Scolytus rugulosus altered by the nematode parasite Neoparasitylenchus rugulosi. Ann Entomol Soc Am 64(3):751

    Article  Google Scholar 

  • Poinar GO Jr, Caylor JN (1974) Neoparasitylenchus amvlocercus sp. n. (Tylenchida: Nematodea) from Conophthorus monophyllae (Scolytidae: Coleoptera) in California with a synopsis of the nematode genera found in bark beetles. J Invertebr Pathol 24(1):112–119

    Article  PubMed  Google Scholar 

  • Polovinko GP, Yaroslavtseva ON, Teshebaeva ZA, Kryukov VY (2010) Dominating species of Entomophilous ascomycetes anamorphs in West Siberia, Primorsky Krai, and Kyrgyzstan. Contemp Probl Ecol 3(5):515–521

    Article  Google Scholar 

  • Purrini K (1978) Protozoen als Krankheitserreger bei einigen Borkenkäferarten (Col., Scolytidae) im Königsee-Gebeit, Oberbayern. Anz Schädlingskunde, Pflanzenschutz, Umweltschutz 51:171–175

    Article  Google Scholar 

  • Purrini K (1981) Nosema hylobii n. sp. (Nosematidae, Microsporida), a new microsporidan parasite of Hylobius abietis L. (Curculionidae, Coleoptera). Z Angew Entomol 92:1–8

    Article  Google Scholar 

  • Purrini K, Halperin J (1982) Nosema calcarati n. sp. (Microsporidia), a new parasite of Pityogenes calcaratus Eichhof (Col., Scolytidae). Z Angew Entomol 94:87–92

  • Purrini K, Ormieres R (1981) On three new sporozoan parasites of bark beetle (Col., Scolytidae). Z Angew Entomol 91:67–74

    Article  Google Scholar 

  • Richardson KC, Jarrett L, Finke EH (1960) Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol 35:313–323

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Samson RA, Evans HC, Latgé J-P (1988) Atlas of entomopathogenic fungi. Springer, Berlin - Heidelberg

  • Schvester D (1950) Sur un nématode du groupe des Parasitylenchus dispar Fuchs, parasite nouveau du Xylebore disparate (Xyleborus dispar F.). Annales de l'Institut national de la recherche agronomique. Serie C. Annales des épiphyties, Paris 1:48–53

    Google Scholar 

  • Schvester D (1957) Contribution a l’étude de coléoptères scolytides. Annales de l'Institut national de la recherche agronomique. Serie C. Annales des épiphyties, Paris 8:1–162

    Google Scholar 

  • Seinhorst JW (1959) A rapid method for the transfer of nematodes from fixative to anhydreous glycerin. Nematologica 4:67–69

    Article  Google Scholar 

  • Takov D, Pilarska D, Wegensteiner R (2006) Оccurrence of pathogens in Ips typographus (Coleoptera, Scolytidae) from several Picea abies (L.) (Karst.) stands in Bulgaria. Acta zool bulg 58(3):409–420

    Google Scholar 

  • Takov D, Doychev D, Wegensteiner R, Pilarska D (2007) Study on the pathogens of bark beetles (Coleoptera, Scolytidae) from different coniferous stands in Bulgaria. Acta zool bulg 59(1):87–96

    Google Scholar 

  • Takov D, Pilarska D, Wegensteiner R (2010) List of protozoan and microsporidian pathogens of economically important bark beetle species (Coleoptera, Curculionidae: Scolytinae) in Europe. Acta zool bulg 62(2):201–209

    Google Scholar 

  • Takov D, Doychev D, Linde A, Draganova S, Pilarska D (2011) Pathogens of bark beetles (Coleoptera: Curculionidae) in Bulgarian forests. Phytoparasitica 39(4):343–352. https://doi.org/10.1007/s12600-011-0167-3

    Article  Google Scholar 

  • Takov D, Doychev D, Linde A, Draganova S, Pilarska D (2012) Pathogens of bark beetles (Curculionidae: Scolytinae) and other beetles in Bulgaria. Biologia 67(5):966–972. https://doi.org/10.2478/s11756-012-0086-x

    Article  Google Scholar 

  • Tomalak M, Welch HE, Gallowayt D (1989) Nematode parasites of bark beetles (Scolytidae) in southern Manitoba, with descriptions of three new species of Sulphuretylenchus Rühm (Nematoda: Allantonematidae). Can J Zool 67:2497–2505

    Article  Google Scholar 

  • Urbanová Z, Urban J (2016) Attelabus nitens (Scop.) – an abundant but biologically little known species from the family of Attelabidae (Coleoptera). Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis 64(5):1675–1696. https://doi.org/10.11118/actaun201664051675

    Article  Google Scholar 

  • Wegensteiner R (1994) Chytridiopsis typographi (protozoa, microsporidia) and other pathogens in Ips typographus (Coleoptera, Scolytidae). IOBC/WPRS Bulletin 17(3):39–42

  • Wegensteiner R (1996) Laboratory evaluation of Beauveria bassiana (Bals.) Vuill. Against the bark beetle, Ips typographus L. (Coleoptera, Scolytidae). IOBC/WPRS Bulletin 19(9):186–189

  • Wegensteiner R (2004) Pathogens in bark beetles. In: Lieutier F, Day K, Battisti A, Gregoire J-C, Evans H (eds) Bark and wood boring insects in living trees in Europe, a synthesis. Kluwer Academic Publishers, Printed in the Netherlands, pp 291–313

    Chapter  Google Scholar 

  • Weiser J (1955) Prispevek k znalosti cizopasniku kurovce Ips typographus, II. (Contributions to the knowledge of Ips typographus parasites, II.). Vestn Ceskoslov Zool Spolec 19:374–380. [in Czech]

  • Weiser J (1961) A new microsporidian from the bark beetle Pityokteines curvidens Germar (Col. Scolytidae) in Czechoslovakia. J Insect Pathol 3:324–329

  • Weiser J (1968) Plistophora scolyti sp. n. (protozoa, microsporidia) a new parasite of Scolytus scolytus F. (Col., Scolytidae). Folia Parasitol 15:11–14

    Google Scholar 

  • Weiser J (1970) Three new pathogens of the Douglas fir beetle, Dendroctonus pseudotsugae: Nosema dendroctoni n. sp., Ophryocystis dendroctoni n. sp., and Chytridiopsis typographi n. comb. J Invertebr Pathol 16(3):436–441

    Article  Google Scholar 

  • Weiser J, Wegensteiner R, Žižka Z (1997) Ultrastructures of Nosema typographi Weiser 1955 (Microspora: Nosematidae) of the bark beetle Ips typographus L. (Coleoptera; Scolytidae). J Invertebr Pathol 70:156–160. https://doi.org/10.1006/jipa.1997.4677

    Article  CAS  PubMed  Google Scholar 

  • Yaman M, Radek R, Tosun O, Ünal S (2009) Nosema raphidiae sp. n. (Microsporida, Nosematidae): a microsporidian pathogen of the predatory Snake-fly Raphidia ophiopsis (Raphidioptera: Raphidiidae). Acta Protozool 48:353–358

    Google Scholar 

Download references

Acknowledgments

We are especially indebted to the National Science Fund of Bulgaria project DO-02-251/2008 and personally to Prof. Renate Radek for her help for TEM of microsporidia. The present study was implemented also with the support of the National Programme of the Bulgarian Ministry of Education and Science “Young Scientists and Postdoctoral Students”.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to D. Doychev.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Takov, D., Doychev, D., Pilarska, D. et al. Occurrence of pathogens and nematodes in forest beetles from Curculionidae and Attelabidae in Bulgaria. Biologia 74, 1339–1347 (2019). https://doi.org/10.2478/s11756-019-00250-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2478/s11756-019-00250-x

Keywords

Navigation