Experimental evidence that fungal symbionts of beetles suppress wood decay by competing with decay fungi

Abstract

Throughout forests worldwide, bark and ambrosia beetles inoculate dead and dying trees with symbiotic fungi. We experimentally determined the effects of three common and widely distributed ascomycete symbionts, and one introduced Asian basidiomycete symbiont on the decay of pine sapwood. Ascomycetes caused less than 5% mass loss and no structural degradation, whereas the basidiomycete Flavodon ambrosius caused nearly 15% mass loss and visible degradation of wood structure. In co-inoculation experiments, the beetle symbionts Ophiostoma ips and Raffaelea fusca reduced white and brown rot decay through competition with Ganoderma curtisii and Phaeolus schweinitzii, respectively. The inhibitory effects of O. ips and R. fusca on decay were negated when co-inoculated with F. ambrosius, suggesting that widespread introduction of this beetle symbiont could alter forest carbon fluxes. In contrast to the predominant forest biology narrative, most bark and ambrosia beetles introduce fungi that delay rather than facilitate tree biomass recycling.

Relationships among wood‐boring beetles, fungi, and the decomposition of forest biomass

“…This inference is supported by the observed density‐dependent relationship between ambrosia beetle galleries and decay, and a lack of a significant relationship between decay and bark beetle galleries. This result is consistent with the localized effects of beetle symbionts observed in vitro (Skelton, Loyd, et al, ). It also provides an explanation for the discrepancies between this study and similar studies which found positive or no significant effects of wood borers on decay in northern temperate forests (Jacobsen, Sverdrup‐Thygeson, Kauserud, Mundra, & Birkemoe, ; Müller et al, ) where ambrosia beetles represent a much smaller fraction of the wood‐borer communities.…”

“…It is also established that beetle‐associated ophiostomataleans quickly consume and degrade available labile carbohydrates and other extractives in fresh wood (Blanchette et al, ; Schirp, Farrell, Kreber, & Singh, ; Wang et al, ). Most importantly, recent laboratory microcosm experiments using co‐inoculations of beetle‐associated fungi and wood decay fungi demonstrated that ophiostomatalean fungal symbionts of bark and ambrosia beetles reduce decay rates of pine sapwood by excluding and/or competing with a common brown rot and a common white rot decay fungus (Skelton, Loyd, et al, ). The in situ study presented here indicates that this symbiont‐mediated suppression of early decay is significant in the field, under conditions of natural complexity.…”

“…For example, several Asian species of the ambrosia beetle genera Ambrosiodmus and Ambrosiophilus have been introduced to multiple continents where they have thrived. Unlike all other ambrosia beetles known, these beetles farm an ambrosia fungus that is an aggressive wood‐decayer which can exclude native fungi, and thus these introduced beetles could potentially offset the effects of native beetles on decay rates (Hulcr, Skelton, Johnson, Li, & Jusino, ; Kasson et al, ; Skelton, Loyd, et al, ). Continued studies of how beetle‐associated fungi interact with free‐living fungi in decaying wood will help clarify the total impact of bark and ambrosia beetle introductions on ecosystem processes in native forests.…”

“…Bark and ambrosia beetles are generally thought to accelerate wood decomposition because they facilitate fungal colonization of wood and increase fungal diversity in early stages of saprotrophic fungal community assembly (Müller, Varama, Heinonen, & Hallaksela, ; Persson, Ihrmark, & Stenlid, ; Strid, Schroeder, Lindahl, Ihrmark, & Stenlid, ; Ulyshen, ). However, the majority of beetle‐associated fungi are not known to decompose lignified cellulose (Kasson et al, ; Skelton, Loyd, et al, ). Instead, these fungi consume labile nonstructural compounds such as sugars (Huang, Skelton, & Hulcr, ; Wang, Lu, Cheng, Salcedo, & Sun, ).…”

“…True decay fungi also utilize these labile resources in addition to more recalcitrant lignocellulose, and competition between nondecay and decay fungi for labile compounds can reduce decay rates (Hulme & Shields, ). Ophiostomatalean fungal symbionts of pine‐infesting bark and ambrosia beetles can compete with wood decaying fungi, excluding them from portions of the wood and limiting wood degradation (Skelton, Loyd, et al, ). Thus, we hypothesized that bark and ambrosia beetles suppress decay of pine sapwood by introducing nondecay fungi during early stages of saprotrophic community assembly, which subsequently compete with wood decay fungi.…”