Skip to main content
SpringerLink
Log in

Symbiotic association of three fungal species throughout the life cycle of the ambrosia beetle Euwallacea nr. fornicatus

  • Published:
Symbiosis Aims and scope Submit manuscript

Abstract

The presence of three symbiotic fungi: Fusarium euwallaceae, Graphium euwallaceae and Acremonium pembeum was detected in the larvae and adult beetles of Euwallacea nr. fornicatus (Coleoptera: Scolytinae) and from the brood galleries of four tree species. Isolations from female beetle mandibular mycangia recovered mainly G. euwallaceae and A. pembeum during adult maturation, whereas isolations from mature adult beetles revealed F. euwallaceae, almost exclusively. Only G. euwallaceae (from adults) and mostly G. euwallaceae (from larvae) were isolated from the guts of the examined beetles. Within larvae, G. euwallaceae was quantified at much higher concentrations for all the tested tree hosts, compared to F. euwallaceae and A. pembeum. Fungal mandibular mycangial loads at each of the adult beetle stages among all tested plant hosts were uniform, while larvae-fungal combinations varied extensively between the sampled sites regardless of the host species; a similar trend of inconsistency for the three fungal combinations was also observed in the galleries. The percentage of feral, naturally occurring, larvae carrying the symbiotic fungi was significantly high, while most of the pupae sampled from these trees did not carry any of the fungi. On artificial rearing medium, larvae fed and completed their development solely on F. euwallaceae and G. euwallaceae but not on A. pembeum. Laboratory-reared larvae fed with a single fungus harbored the other fungi as well. The occurrences and roles of F. euwallaceae, G. euwallaceae and A. pembeum in the beetle developmental stages and in the host trees, along with the life cycle of the beetle, are discussed.

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
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Alamouti SM, Tsui CKM, Breuil C (2009) Multigene phylogeny of filamentous ambrosia fungi associated with ambrosia and bark beetles. Mycol Res 113:822–835

    Article  CAS  Google Scholar 

  • Baker JM, Norris DM (1968) A complex of fungi mutualistically involved in the nutrition of the ambrosia beetle Xyleborus ferrugineus. J Invertebr Pathol 11:246–250

    Article  Google Scholar 

  • Batra LR (1963) Ecology of ambrosia fungi and their dissemination by beetles. Trans Kans Acad Sci 66:213–236

    Article  Google Scholar 

  • Batra LR (1966) Ambrosia fungi: extent of specificity of ambrosia beetles. Science 153:193–195

    Article  CAS  PubMed  Google Scholar 

  • Batra LR (1979) Insect-fungus symbiosis: nutrition, mutualism and commensalism. Wiley, NY

    Google Scholar 

  • Beaver RA (1989) Insect-fungus relationships in the bark and ambrosia beetles. In: Wilding N, Collins NM, Hammond PH, Webber JF (eds) Insect-fungus interactions. Academic, London, pp 121–43

    Chapter  Google Scholar 

  • Biedermann PHW, Klepzig KD, Taborsky M, Six DL (2013) Abundance and dynamics of filamentous fungi in the complex ambrosia gardens of the primitively eusocial beetle Xyleborinus saxesenii Ratzeburg (Coleoptera: Curculionidae, Scolytinae). FEMS Microbiol Ecol 83:711–723

    Article  CAS  PubMed  Google Scholar 

  • Brayford D (1987) Fusarium bugincourtii sp. nov., and its relationship to F. tumidum and F. tumidum var. coeruleum. Trans Br Mycol Soc 89:347–351

    Article  Google Scholar 

  • Cognato AI, Hulcr J, Dole S, Jordal BH (2011) Phylogeny of haplo-diploid, fungus-growing ambrosia beetles (Coleoptera: Curculionidae: Scolytinae: Xyleborini) inferred from molecular and morphological data. Zool Scr 40:174–186

    Google Scholar 

  • Currie CR, Scott JA, Summerbell RC, Malloch D (1999) Fungus growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398:701–704

    Article  CAS  Google Scholar 

  • Danthanarayana W (1968) The distribution and host-range of the shot-hole borer (Xyleborus fornicatus Eichh.) of tea. Tea Q 39:61–69

    Google Scholar 

  • De Fine Licht HH, Biedermann PHW (2012) Patterns of functional enzyme activity in fungus farming ambrosia beetles. Front Zool 9:13–25

    Article  PubMed  PubMed Central  Google Scholar 

  • De Fine Licht HH, Schiøtt M, Mueller UG, Boomsma JJ (2010) Evolutionary transitions in enzyme activity of ant fungus gardens. Evolution 64:2055–2069

    PubMed  Google Scholar 

  • El-Deeb HM, Arab YA (2013) Acremonium as an endophytic bioagent against date palm Fusarium wilt. Arch Phytopathol Plant Prot 46:1214–1221

    Article  CAS  Google Scholar 

  • Eskalen A, Gonzalez A, Wang DH, Twizeyimana M, Mayorquin JS, Lynch SC (2012) First report of a Fusarium sp. and its vector tea shot hole borer (Euwallacea fornicatus) causing Fusarium dieback on avocado in California. Plant Dis 96:1070

    Article  Google Scholar 

  • Eskalen A, Stouthamer R, Lynch SC, Rugman-Jones PF, Twizeyimana M, Gonzalez A, Thibault T (2013) Host range of Fusarium dieback and its ambrosia beetle (Coleoptera: Scolytinae) vector in southern California. Plant Dis 97:938–951

    Article  Google Scholar 

  • Farrell BD, Sequeira AS, O’Meara BC, Normark BB, Chung JH, Jordal BH (2001) The evolution of agriculture in beetles (Curculionidae: Scolytinae and Platypodinae). Evolution 55:2011–2027

    Article  CAS  PubMed  Google Scholar 

  • Fernando EFW (1959) Storage and transmission of ambrosia fungus the adult Xyleborus fornicatus Eich. (Coleoptera: Scolytidae). Ann Mag Nat Hist 13:475–480

    Article  Google Scholar 

  • Francke-Grosmann H (1967) Ectosymbiosis in wood-inhabiting insects. In: Henry SM (ed) Symbiosis, vol II. Academic, New York, pp 171–180

    Google Scholar 

  • Freeman S, Protasov A, Sharon M, Mohotti K, Eliyahu M, Okon-Levy N, Mendel Z (2012) Obligate feed requirement of Fusarium sp. nov., an avocado wilting agent, by the ambrosia beetle Euwallacea aff. fornicata. Symbiosis 57:245–251

    Article  Google Scholar 

  • Freeman S, Sharon M, Maymon M, Mendel Z, Protasov A, Aoki T, Eskalen A, O’Donnell K (2013) Fusarium euwallaceae sp. nov.—a symbiotic fungus of Euwallacea sp., an invasive ambrosia beetle in Israel and California. Mycologia 105:1595–1606

    Article  CAS  PubMed  Google Scholar 

  • Gadd CH, Loos CA (1947) The ambrosia fungus of Xyleborus fornicatus Eich. Trans Br Mycol Soc 31:13–18

    Article  Google Scholar 

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

    Google Scholar 

  • Hulcr J, Cognato AI (2010) Repeated evolution of crop theft in fungus-farming ambrosia beetles. Evolution 64:3205–3212

    Article  PubMed  Google Scholar 

  • Hulcr J, Mogia M, Isua B, Novotny V (2007) Host specificity of ambrosia and bark beetles (Col., Curculionidae: Scolytinae and Platypodinae) in a New Guinea rain forest. Ecol Entomol 32:762–772

    Article  Google Scholar 

  • Jordal BH, Cognato AI (2012) Molecular phylogeny of bark and ambrosia beetles reveals multiple origins of fungus farming during periods of global warming. BMC Evol Biol 12:133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kajimura H, Hijii N (1992) Dynamics of the fungal symbionts in the gallery system and the mycangia of the ambrosia beetle, Xylosandrus mutilatus (Blandford) (Coleoptera: Scolytidae) in relation to its life history. Ecol Res 7:107–117

    Article  Google Scholar 

  • Kasson MT, O’Donnell K, Rooney AP, Sink S, Ploetz RC, Ploetz JN, Konkol JL, Carrillo D, Freeman S, Mendel Z, Smith JA, Black A, Hulcr J, Bateman C, Black AW, Campbell PR, Geering ADW, Dann EK, Eskalen A, Mohotti K, Short DPG, Aoki T, Fenstermacher KA, Davis DD, Geiser DM (2013) Phylogenetic diversity of fusaria cultivated by ambrosia beetles in the genus Euwallacea on avocado and other plant hosts. Fungal Genet Biol 56:147–157

    Article  PubMed  Google Scholar 

  • Kellner K, Ishak HD, Linksvayer TA, Mueller UG (2015) Bacterial community composition and diversity in an ancestral ant fungus symbiosis. FEMS Microbiol Ecol. doi:10.1093/femsec/fiv073

    PubMed  Google Scholar 

  • Kessler KJ Jr (1974) An apparent symbiosis between Fusarium fungi and ambrosia beetle causes canker on black walnut stems. Plant Dis Rep 58:1044–1047

    Google Scholar 

  • Kirkendall LR, Biedermann PHW, Jordal BH (2015) Evolution and diversity of bark and ambrosia beetles. In: Vega F, Hofstetter R (eds) Bark beetles: biology and ecology of native and invasive species. Elsevier, Amsterdam, pp 86–156. doi:10.1016/B978-0-12-417156-5.00003-4

    Google Scholar 

  • Klepzig KD, Six DL (2004) Bark beetle-fungal symbiosis: context dependency in complex associations. Symbiosis 37:189–205

    Google Scholar 

  • Kok LT (1979) Lipids of ambrosia fungi and the life of mutualistic beetles. In: Batra LR (ed) Insect-fungus symbiosis. Halsted, Sussex, pp 33–52

    Google Scholar 

  • Kostovcik M, Bateman CC, Kolarik M, Stelinski LL, Jordal BH, Hulcr J (2015) The ambrosia symbiosis is specific in some species and promiscuous in others: evidence from community pyrosequencing. ISME J 9:126–138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuhnholz S, Borden JH, Uzunovic A (2001) Secondary ambrosia beetles in apparently healthy trees; adaptations, potential causes and suggested research. Integr Pest Manag Rev 6:209–219

    Article  Google Scholar 

  • Kumar NS, Hewavitharanage P, Adikaram NKB (1995) Attack on tea by Xyleborus fornicatus: inhibition of the symbiote, Monacrosporium ambrosium, by caffeine. Phytochemistry 40:1113–1116

    Article  CAS  Google Scholar 

  • Kumar NS, Hewavitharanage P, Adikaram NKB (1998) Histology and fungal flora of shot-hole borer beetle (Xyleborus fornicatus) galleries in tea (Camellia sinensis). J Nat Sci Counc Sri Lanka 26:195–207

    Google Scholar 

  • Lynch SC, Twizeyimana M, Mayorquin JS, Wang DH, Na F, Kayim M, Kasson MT, Thu PQ, Bateman C, Rugman-Jones P, Hulcr J, Stouthamer R, Eskalen A (2015) Identification, pathogenicity, and abundance of Acremonium pembeum sp. nov. and Graphium euwallaceae sp. nov.- two newly discovered mycangial associates of the polyphagous shot hole borer (Euwallacea sp.) in California. Mycologia (in press)

  • Mendel Z, Protasov A, Sharon M, Zveibil A, Ben Yehuda S, O’Donnell K, Rabaglia R, Wysoki M, Freeman S (2012) An Asian ambrosia beetle Euwallacea fornicatus and its novel symbiotic fungus Fusarium sp. pose a serious threat to the Israeli avocado industry. Phytoparasitica 40:235–238

    Article  Google Scholar 

  • Norris DM, Baker JK (1967) Symbiosis: effects of a mutualistic fungus upon the growth and reproduction of Xyleborus ferrugineus. Science 156:1120–1122

    Article  CAS  PubMed  Google Scholar 

  • O’Donnell K, Sink S, Libeskind-Hadas R, Hulcr J, Kasson MT, Ploetz RC, Konkol JL, Ploetz JN, Carrillo D, Campbell A, Duncan RE, Liyanage PNH, Eskalen A, Na F, Geiser DM, Bateman C, Freeman S, Mendel Z, Sharon M, Aoki T, Cossé AA, Rooney AP (2015) Discordant phylogenies suggest repeated host shifts in the Fusarium – Euwallacea ambrosia beetle mutualism. Fungal Genet Biol. doi:10.1016/j.fgb.2014.10.014

    Google Scholar 

  • Pliego C, Kanematsu S, Ruano-Rosa D, de Vicente A, Lopez-Herrera C, Cazorla FM, Ramos C (2009) GFP sheds light on the infection process of avocado roots by Rosellinia necatrix. Fungal Genet Biol 46:137–145

    Article  CAS  PubMed  Google Scholar 

  • Ploetz RC, Hulcr J, Wingfield MJ, DeBeer ZW (2013) Destructive tree diseases associated with ambrosia and bark beetles: black swan events in tree pathology? Plant Dis 95:856–872

    Article  Google Scholar 

  • Santos AV, Dillon RJ, Dillon VM, Reynolds SE, Samuels RI (2004) Occurrence of the antibiotic producing bacterium Burkholderia sp. in colonies of the leaf-cutting ant Atta sexdens rubropilosa. FEMS Microbiol Lett 239:319–23

    Article  CAS  PubMed  Google Scholar 

  • SAS Institute Inc (2014) JMP® 11 Scripting Guide, 2nd edn. SAS Institute Inc., Cary, NC

    Google Scholar 

  • Sharon M, Maymon M, Protasov A, Margalit O, Mohotti K, O’Donnell K, Mendel Z, Freeman S (2015) Dissemination of the fungi Fusarium euwallaceae, Graphium sp. and Acremonium sp., in symbiosis with the ambrosia beetle Euwallacea nr. fornicatus. Phytoparasitica 43:378

    Google Scholar 

  • Six DL (2012) Ecological and evolutionary determinants of bark beetle fungus symbioses. Insects 3:339–366

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The authors are grateful to Dr. Hillary Voet, from the Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, for assistance with statistical analyses of the data. The authors also thank Omer Golan from the forest department, KKL, and Avigail Heller and Ronza Amara from the extension service of the Ministry of Agriculture for their assistance. We also express our appreciation to many avocado growers, gardeners and landscape managers who shared valuable information of infested hosts on their properties and allowed us to remove plant materials for this study. This research was partially funded by grant No. 131-1679 from the Chief Scientist of the Ministry of Agriculture and the Israeli avocado growers’, and grant No. 131-1755 from the KKL forest steering committee.

Author information

Authors and Affiliations

  1. Department of Plant Pathology and Weed Research, ARO, The Volcani Center, Bet Dagan, 50250, Israel

    Stanley Freeman, Michal Sharon, Mally Dori-Bachash & Marcel Maymon

  2. Microscopy Unit, Institute of Plant Sciences, ARO, The Volcani Center, Bet Dagan, 50250, Israel

    Eduard Belausov

  3. Avocado Organization, Israeli Plants Board, Bet Dagan, Israel

    Yonatan Maoz

  4. Department of Entomology, ARO, The Volcani Center, Bet Dagan, 50250, Israel

    Omer Margalit, Alex Protasov & Zvi Mendel

  5. The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, 761000, Israel

    Mally Dori-Bachash & Omer Margalit

Authors
  1. Stanley Freeman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michal Sharon
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mally Dori-Bachash
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marcel Maymon
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Eduard Belausov
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yonatan Maoz
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Omer Margalit
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Alex Protasov
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Zvi Mendel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stanley Freeman.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Freeman, S., Sharon, M., Dori-Bachash, M. et al. Symbiotic association of three fungal species throughout the life cycle of the ambrosia beetle Euwallacea nr. fornicatus . Symbiosis 68, 115–128 (2016). https://doi.org/10.1007/s13199-015-0356-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13199-015-0356-9

Keywords

Search

Navigation