Induced Terpene Accumulation in Norway Spruce Inhibits Bark Beetle Colonization in a Dose-Dependent Manner

Abstract

BackgroundTree-killing bark beetles (Coleoptera, Scolytinae) are among the most economically and ecologically important forest pests in the northern hemisphere. Induction of terpenoid-based oleoresin has long been considered important in conifer defense against bark beetles, but it has been difficult to demonstrate a direct correlation between terpene levels and resistance to bark beetle colonization.MethodsTo test for inhibitory effects of induced terpenes on colonization by the spruce bark beetle Ips typographus (L.) we inoculated 20 mature Norway spruce Picea abies (L.) Karsten trees with a virulent fungus associated with the beetle, Ceratocystis polonica (Siem.) C. Moreau, and investigated induced terpene levels and beetle colonization in the bark.ResultsFungal inoculation induced very strong and highly variable terpene accumulation 35 days after inoculation. Trees with high induced terpene levels (n = 7) had only 4.9% as many beetle attacks (5.1 vs. 103.5 attacks m−2) and 2.6% as much gallery length (0.029 m m−2 vs. 1.11 m m−2) as trees with low terpene levels (n = 6). There was a highly significant rank correlation between terpene levels at day 35 and beetle colonization in individual trees. The relationship between induced terpene levels and beetle colonization was not linear but thresholded: above a low threshold concentration of ∼100 mg terpene g−1 dry phloem trees suffered only moderate beetle colonization, and above a high threshold of ∼200 mg terpene g−1 dry phloem trees were virtually unattacked.Conclusion/SignificanceThis is the first study demonstrating a dose-dependent relationship between induced terpenes and tree resistance to bark beetle colonization under field conditions, indicating that terpene induction may be instrumental in tree resistance. This knowledge could be useful for developing management strategies that decrease the impact of tree-killing bark beetles.

Defence reactions of mature Norway spruce (Picea abies) before and after inoculation of the blue-stain fungus Endoconidiophora polonica in a drought stress experiment

“…We assume that the increased resin flow in September 2014 observed in fully covered spruce trees of the Rosalia roof experiment was also due to the formation of traumatic resin ducts, stimulated by wounding and necrosis. Strong stimulation of tree defences can prevent trees from being successfully mass attacked by bark beetles (Zhao et al 2011), but might also speed up the exhaustion of carbon resources, as argued by Lieutier et al (2009).…”

“…The fungal species therefore has been widely used to study the resistance of Norway spruce and its defence mechanisms in the phloem and xylem in low density and mass inoculation experiments (e.g. Christiansen & Glosli 1996;Krokene et al 1999;Baier et al 2002;Zhao et al 2011;Skrøppa et al 2015).…”

“…Extended drought stress lasting several years eventually involves structural changes such as a reduction in number and size of resin ducts (Ferrenberg et al 2015). Trees that are more resistant show significantly higher terpene levels following inoculation of E. polonica in the dark coloured zone around the entrance hole penetrated by fungal hyphae (Zhao et al 2011). Concentrations and composition of particular phenols can even predict Norway spruce resistance to inoculation of E. polonica as shown by Brignolas et al (1995Brignolas et al ( , 1998.…”

Catechol dioxygenases catalyzing the first step in Norway spruce phenolic degradation are key virulence factors in the bark beetle-vectored fungus Endoconidiophora polonica

“…Under severe infestation, this can lead to tree mortality. Fungal infestation is hypothesized to enhance bark beetle brood development by exhausting the tree's defenses at an early stage during host colonization (Paine et al, 1997;Solheim, 1998, 2001;Nagy et al, 2004;Franceschi et al, 2005;Zhao et al, 2011).…”

Overexpression of an Isoprenyl Diphosphate Synthase in Spruce Leads to Unexpected Terpene Diversion Products That Function in Plant Defense

“…that are stored in specialized resin ducts and deter insects such as bark beetles and their associated fungi (Erbilgin et al, 2006;Bohlmann, 2006a, 2006b;Zhao et al, 2011;Schiebe et al, 2012). The oleoresin is composed mainly of monoterpenes (C 10 ) and diterpene acids (C 20 ), with very minor amounts of sesquiterpenes (Martin et al, 2002).…”