Skip to main content
Log in

Fungal symbionts in three exotic ambrosia beetles, Xylosandrus amputatus, Xyleborinus andrewesi, and Dryoxylon onoharaense (Coleoptera: Curculionidae: Scolytinae: Xyleborini) in Florida

  • Published:
Symbiosis Aims and scope Submit manuscript

Abstract

In nearly every forest habitat, ambrosia beetles (Coleoptera: Curculionidae: Scolytinae, Platypodinae) plant and maintain symbiotic fungus gardens inside dead or dying trees. Some non-native ambrosia beetles aggressively attack live trees and damage tree crops, lumber, and native woody plant taxa by introducing ambrosia fungi, some of which are plant pathogens. Most established exotic species, however, do not cause any economic damage, and consequently are little studied. To determine the specificity and diversity of ambrosia symbionts in under-studied non-native beetles in Florida, fungi were isolated from three species: Xylosandrus amputatus, Xyleborinus andrewesi, and Dryoxylon onoharaense. Two of the beetles sampled each yielded a fungal species isolated with 100 % frequency: X. amputatus: Ambrosiella beaveri or A. nakashimae, and X. andrewesi: Raffaelea sp. nov. nr. canadensis. Both of these symbionts have been isolated previously from closely related ambrosia beetles, supporting the hypothesis that some beetles can carry monocultures of fungi, but the fungi may not be specific to single beetle species. No consistent fungi were isolated from Dryoxylon onoharaense, raising questions about whether or not it truly carries its own symbionts. These results are now being used to test hypotheses and models explaining the evolution of pathogenicity within ambrosia fungi and invasion ability within exotic beetle-fungus complexes.

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

Similar content being viewed by others

References

  • Ayres MP, Wilkens RT, Ruel JJ, Lombardero MJ, Vallery E (2000) Nitrogen budgets of phloem-feeding bark beetles with and without symbiotic fungi. Ecology 81(8):2198–2210

    Article  Google Scholar 

  • Batra LR (1963) Ecology of ambrosia fungi and their dissemination by beetles. Trans Kans Acad Sci 1903:213–236

    Article  Google Scholar 

  • Batra LR (1966) Ambrosia fungi: extent of specificity to ambrosia beetles. Science 153(3732):193–195

    Article  CAS  PubMed  Google Scholar 

  • Batra LK (1967) Ambrosia fungi: a taxonomic revision, and nutritional studies of some species. Mycologia 59:976–1017. doi:10.2307/3757271

    Article  Google Scholar 

  • Beer ZW d, Duong TA, Barnes I, Wingfield BD, Wingfield MJ (2014) Redefining ceratocystis and allied genera. Stud Mycol. doi:10.1016/j.simyco.2014.10.001

  • Biedermann PH, Klepzig KD, Taborsky M, Six DL (2013) Abundance and dynamics of filamentous fungi in the complex ambrosia gardens of the primitively eusocial beetle xyleborinus saxeseniiRatzeburg (coleoptera: curculionidae, scolytinae). FEMS Microbiol Ecol 83(3):711–723

    Article  CAS  PubMed  Google Scholar 

  • Brader L (1964) Etude de la relation entre le scolyte des rameaux du caféier xyleborus compactus eichh. X Morstatti 1-109

  • Bright DE, Rabaglia RJ (1999) Dryoxylon, a new genus for xyleborus onoharaensis Murayama, recently established in the southeastern United States (coleoptera: scolytidae). Coleopt Bull 333-337

  • Carrillo D, Duncan RE, Ploetz JN, Campbell AF, Ploetz RC, Peña JE (2014) Lateral transfer of a phytopathogenic symbiont among native and exotic ambrosia beetles. Plant Pathol 63(1):54–62. doi:10.1111/ppa.12073

    Article  Google Scholar 

  • Cognato AI, Hulcr J, Dole SA, Jordal BH (2011a) Phylogeny of haplo–diploid, fungus-growing ambrosia beetles (curculionidae: scolytinae: xyleborini) inferred from molecular and morphological data. Zool Scr 40(2):174–186

    Google Scholar 

  • Cognato AI, Olson RO, Rabaglia RJ (2011b) An Asian ambrosia beetle, xylosandrus amputatus (blandford) (curculionidae: scolytinae: xyleborini), discovered in Florida, U.S.A. Coleopt Bull 65(1):43–45

    Article  Google Scholar 

  • Coppedge BR, Stephen FM, Felton GW (1995) Variation in female southern pine beetle size and lipid content in relation to fungal associates. The Canadian Entomologist 127(02):145–154

    Article  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) JModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9(8):772

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dole SA, Cognato AI (2010) Phylogenetic revision of xylosandrus reitter (coleoptera: curculionidae: scolytinae: xyleborina). Proceedings of the California Academy of Sciences

  • Dreaden TJ, Davis JM, De Beer ZW, Ploetz RC, Soltis PS, Wingfield MJ, Smith JA (2014) Phylogeny of ambrosia beetle symbionts in the genus raffaelea. Fungal Biology 118(12):970–978

    Article  PubMed  Google Scholar 

  • Francke-Grosmann H (1967) Ectosymbiosis in wood-inhabiting insects. Symbiosis 2:141–205

    Article  Google Scholar 

  • Fox JW, Wood DL, Akers RP, Parmeter JR (1992) Survival and development of Ips paraconfusus Lanier (coleoptera: scolytidae) reared axenically and with tree-pathogenic fungi vectored by cohabiting dendroctonus species. The Canadian Entomologist 124(06):1157–1167

    Article  Google Scholar 

  • Glass NL, Donaldson GC (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol 61:1323–1330

  • Guindon S, Gascuel O (2003) A simple, fast and accurate method to estimate large phylogenies by Maximum-likelihood". Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59(3):307–321

  • Haack RA, Rabaglia RJ (2013) Exotic bark and ambrosia beetles in the USA: potential and current invaders. Potential Invasive Pests of Agricultural Crops. CAB International, Boston, MA, pp. 48–74

    Google Scholar 

  • Harrington TC, Aghayeva DN, Fraedrich SW (2010) New combinations in raffaelea, ambrosiella, and hyalorhinocladiella, and four new species from the redbay ambrosia beetle, xyleborus glabratus. Mycotaxon 111(1):337–361

    Article  Google Scholar 

  • Harrington TC, Yun HY, Lu SS, Goto H, Aghayeva DN, Fraedrich SW (2011) Isolations from the redbay ambrosia beetle, xyleborus glabratus, confirm that the laurel wilt pathogen, raffaelea lauricola, originated in Asia. Mycologia 103(5):1028–1036

    Article  PubMed  Google Scholar 

  • Harrington, T. C., McNew, D., Mayers, C., Fraedrich, S. W., & Reed, S. E. (2014). Ambrosiella roeperi sp. nov. is the mycangial symbiont of the granulate ambrosia beetle, Xylosandrus crassiusculus. Mycologia, 106(4), 835845. doi:10.3852/13-354

  • Hofstetter RW, Cronin JT, Klepzig KD, Moser JC, Ayres MP (2006) Antagonisms, mutualisms and commensalisms affect outbreak dynamics of the southern pine beetle. Oecologia 147(4):679–691

    Article  PubMed  Google Scholar 

  • Hulcr J, Cognato AI (2010) Repeated evolution of crop theft in fungus-farming ambrosia beetles. Evolution 64(11):3205–3212

    Article  PubMed  Google Scholar 

  • Hulcr J, Dunn RR (2011) The sudden emergence of pathogenicity in insect-fungus symbioses threatens naive forest ecosystems. Proceedings Biological sciences/The Royal Society 278(1720):2866–2873. doi:10.1098/rspb.2011.1130

    Article  PubMed Central  PubMed  Google Scholar 

  • Jari Oksanen, F. Guillaume Blanchet, Roeland Kindt, Pierre Legendre, Peter R. Minchin, R. B. O'hara, Gavin L. Simpson, Peter Solymos, M. Henry H. Stevens And Helene Wagner (2015). Vegan: community ecology package. R package version 2.2–1. http://cran.r-project.org/package=vegan

  • Kasson MT, O'Donnell K, Rooney AP, Sink S, Ploetz R, Ploetz JN, Konkol JN, Carillo D, Freeman S, Mendel Z, Smith JE, Black A, Hulcr J, Bateman C, Black AW, Campbell PR, Geering AD, Dann EK, Eskalen A, Mohotti K, Short DP, Aoki T, Fenstermacher KA, Davis DD, Geiser DM (2013) An inordinate fondness for fusarium: phylogenetic diversity of fusaria cultivated by ambrosia beetles in the genus euwallacea on avocado and other plant hosts. Fungal Genet Biol: FG & B 56:147–157. doi:10.1016/j.fgb.2013.04.004

    Article  Google Scholar 

  • Kendra PE, Montgomery WS, Sanchez JS, Deyrup MA, Niogret J, Epsky ND (2012) Method for collection of live redbay ambrosia beetles, xyleborus glabratus (coleoptera: curculionidae: scolytinae). Florida Entomol 95(2):513–516

    Article  Google Scholar 

  • Kendra PE, Niogret J, Montgomery WS, Deyrup MA, Epsky ND (2015) Cubeb oil lures: terpenoid emissions, trapping efficacy, and longevity for attraction of redbay ambrosia beetle (coleoptera: curculionidae: scolytinae). J Econ Entomol 108(1):350–361

    Article  PubMed  Google Scholar 

  • Kim JJ, Lim Y, Wingfield M, Breuil C, Kim GH (2004) Leptographium bistatum sp. nov., a new species with a Sporothrix synanamorph from Pinus radiata in Korea. Mycol Res 108:699–706

  • Kostovcik M, Bateman CC, Kolarik M, Stelinski LL, Jordal BH, Hulcr J (2014) The ambrosia symbiosis is specific in some species and promiscuous in others: evidence from community pyrosequencing. ISME J

  • Kubono T, Ito SI (2002) Raffaelea quercivora sp. nov. associated with mass mortality of Japanese oak, and the ambrosia beetle (platypus quercivorus). Mycoscience 43(3):0255–0260

    Article  Google Scholar 

  • Li, Y., Simmons, D.R., Bateman, C., Short, D.P., Kasson, M.T., Rabaglia, R., Hulcr, J. (2015). New fungus-insect symbiosis: culturing, molecular, and histological methods determine saprophytic Polyporales mutualists of Ambrosiodmus. PLoS One. Sep 14;10(9):e0137689.

  • Massoumi Alamouti S, Tsui CK, Breuil C (2009) Multigene phylogeny of filamentous ambrosia fungi associated with ambrosia and bark beetles. Mycol Res 113(Pt 8):822–835. doi:10.1016/j.mycres.2009.03.003

    Article  PubMed  Google Scholar 

  • Mayers CG, Mcnew DL, Harrington TC, Roeper RA, Fraedrich SW, Biedermann PH, Castrillo LA, Reed SE (2015) Three genera in the ceratocystidaceae are the respective symbionts of three independent lineages of ambrosia beetles with large, complex mycangia. Fungal Biology

  • Mueller UG, Gerardo N (2002) Fungus-farming insects: multiple origins and diverse evolutionary histories. P Natl Acad Sci USA 99(24):15247–15249. doi:10.1073/pnas.242594799

    Article  CAS  Google Scholar 

  • Mueller, U. G., Gerardo, N. M., Aanen, D. K., Six, D. L., & Schultz, T. R. (2005). The evolution of agriculture in insects. Annu Rev Ecol Evol S 563-595.

  • Nobre T, Koné NA, Konaté S, Linsenmair KE, Aanen DK (2011) Dating the fungus-growing termites' mutualism shows a mixture between ancient codiversification and recent symbiont dispersal across divergent hosts. Mol Ecol 20(12):2619–2627. doi:10.1111/j.1365-294x.2011.05090.x

    Article  CAS  PubMed  Google Scholar 

  • Okins KE, Thomas MC (2010) New north American record for xyleborinus andrewesi (coleoptera: curculionidae: scolytinae). Florida Entomol 93(1):133–134

    Article  Google Scholar 

  • Schiefer TL (2015) A new earliest date of first detection for the exotic ambrosia beetle dryoxylon onoharaense (Murayama)(coleoptera: curculionidae: scolytinae) in North America. Coleopt Bull 69(1):178–179

    Article  Google Scholar 

  • Six DL, Paine TD (1998) Effects of mycangial fungi and host tree species on progeny survival and emergence of dendroctonus ponderosae (coleoptera: scolytidae). Environ Entomol 27(6):1393–1401

    Article  Google Scholar 

  • Six DL, Stone WD, de Beer ZW, Woolfolk SW (2009) Ambrosiella beaveri, sp. nov., associated with an exotic ambrosia beetle, xylosandrus mutilatus (coleoptera: curculionidae, scolytinae), in Mississippi, USA. A Van Leeuw J Microb 96(1):17–29

    Article  Google Scholar 

  • White TJ, Bruns T, Lee SJWT, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: A Guide to Methods and Applications 18:315–322

  • Wood SL (1982) The bark and ambrosia beetles of north and central America (coleoptera: scolytidae), a taxonomic monograph. Great Basin Nat Mem 6:1–1356

    Google Scholar 

Download references

Acknowledgments

We thank Wayne Montgomery, Chris Gibbard and Lukasz Stelinski for aid in beetle collections.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jiri Hulcr.

Ethics declarations

Competing interests

RR works for the U.S. Forest service which partly funded this study. CCB, PEK, JH declare no competing interests.

Funding

This study was funded by United States Department of Agriculture (USDA) Forest Service (FS)-SRS Coop agreement 14-CA-11,330,130-032, USDA-FS-FHP Coop agreement 12-CA-11,420,004-042, USDA Farm Bill agreement 14–8130-0377-CA, National Science Foundation DEB 1256968, and a University of Florida Opportunity Seed fund.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bateman, C., Kendra, P.E., Rabaglia, R. et al. Fungal symbionts in three exotic ambrosia beetles, Xylosandrus amputatus, Xyleborinus andrewesi, and Dryoxylon onoharaense (Coleoptera: Curculionidae: Scolytinae: Xyleborini) in Florida. Symbiosis 66, 141–148 (2015). https://doi.org/10.1007/s13199-015-0353-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13199-015-0353-z

Keywords

Navigation