Abstract
We examined the interaction between host trees and fungi associated with a tree-killing bark beetle, Dendroctonus frontalis. We evaluated (1) the response of four Pinus species to fungal invasion and (2) the effects of plant secondary metabolites on primary growth of and secondary colonization of three consistent fungal associates. Two of these fungi, Entomocorticium sp. A and Ophiostoma ranaculosum, are obligate mutualists with D. frontalis, and the third associate is a blue-staining fungus, O. minus, that is commonly introduced by beetles and phoretic mites. O. minus negatively affects beetle larvae and in high abundance can impact D. frontalispopulation dynamics. Size of lesions formed and quantity of secondary metabolites produced in response to fungal inoculations varied significantly among Pinus species. However, monoterpene composition within infected tissue did not significantly vary across treatments. While all eight tested metabolites negatively affected the growth rate of O. minus, only 4-allylanisole, p-cymene, and terpinene reduced the growth of the mycangial fungi. Surprisingly, growth rates of mycangial fungi increased in the presence of several secondary metabolite volatiles. O. minus out-competed both mycangial fungi, but the presence of secondary metabolites altered the outcome slightly. O. ranaculosum out-performed E. sp. A in the presence of dominant conifer monoterpenes, such as α- and β-pinene. Volatiles from the mycangial fungi, particularly E. sp. A, had a negative effect on O. minus growth. In general, phloem phytochemistry of particular Pinus species appeared to alter the relative growth and competitiveness of mutualistic and non-mutualistic fungi associated with D. frontalis. The outcome of interactions among these fungi likely has important consequences for the population dynamics of D. frontalis.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
AYRES, M. P., WILKENS, R. T., RUEL, J. J., LOMBARDERO, M. J., and VALLERY, E. 2000. Nitrogen budgets of phloem-feeding bark beetles with and without symbiotic fungi (Coleoptera: Scolytidae). Ecology 81:2198–2210.
BARRAS, S. J. 1970. Antagonism between Dendroctonus frontalis and the fungus Ceratocystis minor. Ann. Entomol. Soc. Am. 63:1187–1190.
BARRAS, S. J. 1973. Reduction in progeny and development in the southern pine beetle following removal of symbiotic fungi. Can. Entomol. 105:1295–1299.
BARRAS, S. J. and PERRY, T. 1972. Fungal symbionts in the prothoracic mycangium of Dendroctonus frontalis (Coleoptera: Scolytidae). Z. Ang. Entomol. 71:95–104.
BEAVER, R. D. 1989. Insect-fungus relationships in the bark and ambrosia beetles, pp. 121–143, in N., Wilding, N. M., Collins, P. M., Hammond, and J. F. Webber, (eds.). Insect-Fungus Interactions. London.
BERRYMAN, A. A. 1972. Resistance of conifers to invasion of bark beetle–fungus associations. Bioscience 22:598–602.
BOBBY, L. 2000. Interspecific combative interactions between wood-decaying Basidiomycetes. FEMS Microbiology Ecology 31:185–194.
BRIDGES, J. R. 1983. Mycangial fungi of Dendroctonus frontalis (Coleoptera: Scolytidae) and their relationship to beetle population trends. Environ. Entomol. 12:858–861.
BRIDGES, J. R. 1987. Effects of terpenoid compounds on growth of symbiotic fungi associated with the southern pine beetle. Phytopathology 77:83–85.
BRIDGES, J. R., NETTLETON, W. A., and CONNOR, M. D. 1985. Southern pine beetle (Coleoptera: Scolytidae) infestations without the bluestain fungus, Ceratocystis minor. J. Econ. Entomol. 78:325–327.
BRIDGES, J. R. and PERRY, T. 1985. Effects of mycangial fungi on gallery construction and distribution of bluestain in southern pine beetle infested pine bolts. J. Entomol. Sci. 20:271-275.
BRIDGES, J. R. and MOSER, J. C. 1986. Relationship of phoretic mites (Acari: Tarsonemidae) to the bluestaining fungus, Ceratocystis minor, in trees infested by southern pine beetle (Coleoptera: Scolytidae). Envir. Entomol. 15:951–953.
CHRISTIANSEN, E. 1985. Ceratocystis polonica inoculated in Norway spruce: blue-staining in relation to inoculatum density, resinosis and tree growth. Eur. J. For. Pathol. 15:160–167.
CHRISTIANSEN, E. and HORNTVEDT, R. 1983. Combined Ips/Ceratocystis attack on Norway spruce, and defensive mechanisms of the trees. Z. Ang. Entomol. 96:110–118.
CHRISTIANSEN, E., WARING, R. H., and BERRYMAN, A. A. 1987. Resistance of conifers to bark beetle attack: searching for general relationships. For. Ecol. Manage. 22:89–106.
COBB, F. W. JR., KRSTIC, M., ZAVARIN, E., and BARBER, H. W. JR. 1968. Inhibitory effects of volatile oleoresin components on Fomes annosus and four Ceratocystis species. Phytopathology 58:1199–1324.
COOK, S. P. and HAIN, F. P. 1985. Qualitative examination of the hypersensitive response of loblolly pine, Pinus taeda L., inoculated with two fungal associates of the southern pine beetle, Dendroctonus frontalis Zimmermann (Coleoptera: Scolytidae). Environ. Entomol. 14:396–400.
COOK, S. P. and HAIN, F. P. 1987. Wound response of loblolly and shortleaf pine attacked or reattacked by D. frontalis or its fungal associate, C. minor. Can. J. For. Res. 18:33–37.
COPPEDGE, B. R., STEPHEN, F. M., and FELTON, G. W. 1995. Variation in female southern pine beetle size and lipid content in relation to fungal associates. Can. Entomol. 127:145-154.
COULSON, R. N. and WITTER, J. A. 1984. Forest Entomology: Ecology and Management. 669 pages. John Wiley & Sons, Inc.
COYNE, J. F. and LOTT, L. H. 1976. Toxicity of substances in pine oleoresin to southern pine beetles. J. Ga. Entomol. Soc. 11:301–305.
DELORME, L. and LIEUTIER, F. 1990. Monoterpene composition of the preformed and induced resins of Scots pine, and their effect on bark beetles and associated fungi. European Journal of Forest Pathology 20:304–316.
FRANCESCHI, V. R., KROKENE, P., KREKLING, T., and CHRISTIANSEN, E. 2000. Phloem parenchyma cells are involved in local and distant defense responses to fungal inoculation or bark-beetle attack in Norway spruce (Pinaceae). Amer. J. Bot. 87:314–326.
FRANCKE-GYROSMANN, H. 1967. Ectosymbiosis in wood inhabiting insects, pp. 141–205, in S. M. Henry (ed.). Symbiosis, Vol. 2 New York Academic, N.Y.
GOLDHAMMER, D. S., STEPHEN, F. M., and PAINE, T. D. 1989. Average radial growth rate and chlamydospore production of Ceratocystis minor, Ceratocystis minor var. barrasii, and SJB 122 in culture. Can. J. Bot. 67:3498–3505.
GOLDHAMMER, D. S., STEPHEN, F. M., and PAINE, T. D. 1990. The effect of the fungi Ceratocystis minor (Hedgecock) Hunt, Ceratocystis minor (Hedgecock) Hunt var barrasii Taylor, and SJB 122 on reproduction of the southern pine beetle, Dendroctonus frontalis Zimmermann (Coleoptera: Scolytidae). Can. Entomol. 122:407–418.
HARRINGTON, T. C. 1993. Biology and taxonomy of fungi associated with bark beetles, pp. 37–58, in T. D. Schowalter, G. M. Filip (eds.). Beetle-Pathogen Interactions in Conifer Forests. Academic Press, San Diego, California.
HODGES, J. D., ELAM, W. W., WATSON, W. F., and NEBEKER, T. E. 1979. Oleoresin characteristics and susceptibility of four southern pines to southern pine beetle (Coleoptera: Scolytidae) attacks. Can. Ent. 111:889–896.
HODGES, J. D., NEBEKER, T. E., DEANGELIS, J. D., KARR, B. L., and BLANCHE, C. A. 1985. Host resistance and mortality: a hypothesis based on the southern pine beetle-microorganism-host interactions. Bull. Entomol. Soc. Am. 31:31–35.
HOFSTETTER, R. W. 2004. Interspecific interactions and population dynamics of the southern pine beetle. PhD dissertation. Dartmouth College, Hanover, NH.
JACOBS, K. and WINGFIELD, M. J. 2001. Leptographium Species: Tree Pathogens, Insect Associations, and Agents of Blue-Stain. The American Phytopathological Society, St. Paul, Minnesota.
KREBER, B. and BYRNE, A. 1994. Discolorations of Hem-Fir wood–a review of the mechanisms. Forest Products. 44:35–42.
KLEPZIG, K. D. and WILKENS, R. T. 1997. Competitive interactions among symbiotic fungi of the southern pine beetle. Appl. Environmental Microbiology 63:621–627.
KLEPZIG, K. D. and WALKINSHAW, C. H. 2003. Cellular response of loblolly pine to wound inoculation with bark beetle-associated fungi and chitosan. USDA Forest Service, Southern Research Station, Research Paper SRS-30. 9 p.
KNOBLOCH, K., PAULI, A., IBERL, B., WEIS, N., and WEIGARD, H. 1989. Antibacterial and antifungal properties of essential oil components. J. Essent. Oil Res. 1:119–128.
LIEUTIER, F. and FERRELL, G. T. 1988. Relationships between indexes of tree vigour and the induced reaction of Scots pine to a fungus associated with Ips sexdentatus Boern. (Coleoptera: Scolytidae), pp. 163–178, in T. L. Payne and H. Saarenmaa (eds.). Integrated Control of Scolytid Bark Beetles. Blacksburg, Virginian Polytechnical Institute State University.
LIEUTIER, F., GARCIA, J., ROMARY, P., YART, A., JACTEL, H., and SAUVARD, D. 1993. Inter-tree variability in the induced defense reaction of Scots pine to single inoculations by Ophiostoma brunneo-ciliatum, a bark beetle-associated fungus. For. Ecol. Manag. 59:257–270.
LOMBARDERO, M. J., AYRES, M. P., LORIO, P. L. JR., and RUEL, J. J. 2000. Environmental effects in constitutive and inducible resin defences of Pinus taeda. Ecol. Letters 3:329–339.
LOMBARDERO, M. J., AYRES, M. P., HOFSTETTER, R. W., MOSER, J. C., and KLEPZIG, K. D. 2003. Strong indirect interactions of Tarsonemus mites (Acrina: Tarsonemidae) and Dendroctonus frontalis (Coleoptera: Scolytidae). Oikos 102:243–252.
NEBEKER, T. E., HODGES, J. D., and BLANCHE, C. A. 1993. Host response to bark beetle and pathogen colonization, pp. 157–173, in T. D. Schowalter and G. M. Filip (eds.). Beetle-Pathogen Interactions in Conifer Forests. Academic Press, San Diego, California.
NELSON, R. M., ORR, L. W., and CHRISTENSEN, C. 1934. The interrelationships of bark beetles and blue-staining fungi in felled Norway pine timber. J. Agric. Res. 49:315–342.
PAINE, T. D. 1984. Seasonal response of ponderosa pine to inoculation of the mycangial fungi from the eastern pine beetle. Can. J. Bot. 62:551–555.
PAINE, T. D. and STEPHEN, F. M. 1987. Fungi associated with the southern pine beetle: avoidance of induced defense response in loblolly pine. Oecologia 74:377–379.
PAINE, T. D. and STEPHEN, F. M. 1988. Induced defenses of loblolly pine, Pinus taeda: potential impact on Dendroctonus frontalis within-tree mortality. Entomol. Exp. Appl. 46:39–46.
PAINE, T. D. and HANLON, C. C. 1994. Influence of oleoresin constituents from Pinus ponderosa and Pinus jeffreyi on growth of mycangial fungi from Dendroctonus ponderosae and Dendroctonus jefferyi. J. Chem. Ecol. 20:2551–2563.
PAINE, T. D., RAFFA, K. F., and HARRINGTON, T. C. 1997. Interactions among scolytid bark beetles, their associated fungi, and live host conifers. Annu Rev. Entomology 42:179–206.
PAYNE, T. L., COSTER, J. E., RICHERSON, J. V., EDSON, L. J., and HART, E. R. 1978. Field response of the southern pine beetle to behavioral chemicals. Environ. Entomol. 7:578–582.
PEARL, I. A. 1975. Variation of loblolly and slash pine bark extractive components and wood turpentine components on a monthly basis. Tappi 58:146–149.
PORTER, C. L. 1924. Concerning the characters of certain fungi as exhibited by their growth in the presence of other fungi. Am. J. Botany 24:168–188.
PRICE, T. S. and DOGGETT, C. 1978. A History of Southern Pine Beetle Outbreaks in the Southeastern United States. Georgia Forestry Commission. Macon, GA.
RAFFA, K. F. 2001. Mixed messages across multiple trophic levels: the ecology of bark beetle chemical communication systems. Chemoecology 11:49–65.
RAFFA, K. F. and BERRYMAN, A. A. 1982. Physiological differences between lodgepole pines resistant and susceptible to the mountain pine beetle and associated microorganisms. Environ. Entomol. 11: 486–492.
RAFFA, K. F. and BERRYMAN, A. A. 1983. The role of host plant resistance in the colonization behavior and ecology of bark beetles (Coleoptera: Scolytidae). Ecol. Monographs 53:27–49.
RAFFA, K. F. and SMALLEY, E. B. 1988. Seasonal and long-term responses of host trees to microbial associates of the pine engraver, Ips pini. Can J. For. Res. 18:1624–1634.
RICE, F. F. 1970. Some biological effects of volatiles emanating from wood. Can. J. Bot. 48:719.
ROSS, D. W., FENN, P., and STEPHEN, F. M. 1992. Growth of southern pine beetle associated fungi in relation to the induced wound response in loblolly pine. Can. J. For. Res. 22:1951–1859.
SCHOWALTER, T. D. and FILIP, G. M. 1993. Beetle-Pathogen Interactions in Conifer Forests. Academic Press Limited, San Diego, CA.
SIX, D. 2003. Bark beetle-fungus symbioses, pp. 97–114, in K. Bourtzis and T. Miller (eds.). Insect Symbiosis. CRC Press, Boca Raton, FL.
SIX, D. L. and PAINE, T. D. 1998. Effects of mycangial fungi and host tree species on progeny survival and emergence of Dendroctonus ponderosae (Coleoptera: Scolytidae). Environ. Entomol. 27:1393–1401.
SMITH, R. H. 1963. Toxicity of pine resin vapors to three species of Dendroctonus bark beetles. J. Econ. Entomol. 56:827–831.
SMITH, R. H. 1966. Resin quality as a factor in the resistance of pines to bark beetles, pp. 189–196, in R. H. Smith (ed.). Breeding Pest-Resistant Trees. Pergamon Press, New York.
SOLHEIM, H. 1992. The early stages of fungal invasion in Norway spruce infested by the bark beetle Ips typographus. Can. J. Bot. 70:1–5.
STANTON, M. L. 2003. Interacting guilds: moving beyond the pairwise perspective on mutualisms. Am. Nat. 162:10–23.
STROM, B. L., ROTON, L. M., and INGRAM, L. L. JR. 1994. Repellent properties of the host compound 4-allylanisole to the southern pine beetle. J. Chem. Ecol. 20:1579–1615.
STROM, B. L., CLARKE, S. R., and SHEA, P. J. 2004. Efficacy of 4-allylanisole-based products for protecting individual loblolly pines from Dendroctonus frontalis Zimmermann (Coleoptera: Scolytidae). Can. J. For. Res. 34:659–665.
TISDALE, R. A., NEBEKER, T. E., and HODGES, J. D. 2003. The role of oleoresin flow in the induced response of loblolly pine to a southern pine beetle associated fungus. Can. J. Botany 81:368–374.
TRAPP, S. and CROTEAU, R. 2001. Defensive resin biosynthesis in conifers. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52:689–724.
VEYSEY, J. S., AYRES, M. P., LOMBARDERO, M. J., HOFSTETTER, R. W., and KLEPZIG, K. D. 2003. Relative suitability of Virginia pine and loblolly pine as host species for Dendroctonus frontalis (Coleoptera: Scolytidae). Environ. Entomol. 32:668–678.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hofstetter, R.W., Mahfouz, J.B., Klepzig, K.D. et al. Effects Of Tree Phytochemistry On The Interactions Among Endophloedic Fungi Associated With The Southern Pine Beetle. J Chem Ecol 31, 539–560 (2005). https://doi.org/10.1007/s10886-005-2035-4
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s10886-005-2035-4