Wood-feeding insects face a host of physical, chemical, and nutritional barriers in their food resource. Wood-boring Hymenoptera in the family Siricidae are associated with mutualistic basidiomycete wood-rot fungi, which assist colonization and provide nutrition for their insect partner, though functional properties of this symbiosis are poorly described. In this study, we document the behavioral and morphological adaptations of the globally invasive woodwasp, Sirex noctilio F., for foraging using its fungal symbiont Amylostereum areolatum (Chaillet ex Fries) Boidin. Larvae concentrated foraging near the border of fungal symbiont growth in pine xylem. Foraging larvae do not ingest bulk xylem tissue, but rather use specialized asymmetric mandibles to press xylem shavings and extract liquid fractions. Fluids drain toward the oral cavity via a sulcus on the occlusal surface of the left mandible. Processed shavings are expelled from the oral cavity without ingestion and passed along the underside of the larvae via peristaltic undulation to the rear of the feeding gallery. Larval midguts lack elaborated chambers typical in insects reliant on microbial fermentation of cellulose, and no xylem tissue was recovered from gut dissections. Larval behavior and functional morphology indicate larval S. noctilio do not ingest xylem, but instead use the fungus as an external gut for digestion of recalcitrant lignocellulosic compounds.

Antagonistic species interactions may prevent introduced species from becoming invasive in novel geographic ranges. Within mutualisms, resistance to any partner can impact the mutualism as a whole. Larvae of the globally invasive Sirex woodwasp Sirex noctilio (Hymenoptera: Siricidae) complete their development in the sapwood of Pinus spp. (Pinaceae) only in the presence of the fungus, Amylostereum areolatum (Basidiomycota). In the Southern Hemisphere where Pinus are introduced, Sirex noctilio is an outbreak invasive pest, but in North America where Pinus is indigenous it has not irrupted to economic levels 15+ yr since introduction. To test the biotic resistance hypothesis, we characterized the arthropod community attracted to and co‐infesting Pinus resinosa trees at the geographic frontier of its introduced North American range, quantified antagonistic interactions observed within trees, and assayed competition of fungal species under laboratory conditions. A suite of potential natural enemies and competitors inhabited Sirex‐infested P. resinosa trees. Trees experimentally exposed to ovipositing Sirex noctilio females and to physical wounding attracted greater numbers of saprophagous beetles (Cerambycidae: Xylotrechus sagittatus and Curculionidae: Ips pini) and parasitoid wasps (Ichneumonidae: Ibalia leucospoides) compared to undamaged controls. Recruitment of Xylotrechus and Ibalia was positively related to numbers of oviposition scars left by Sirex females. Within xylem tissue, abundant Xylotrechus larvae killed and consumed more than 10% of Sirex larvae. This facultative intraguild predation was positively density‐dependent but nonlinear, with a unimodal peak at intermediate Sirex density. Sirex density in xylem was weakly, negatively related to Ips bark beetle density, suggesting potential competition between fungal associates (Ascomycota: Ophiostoma ips) for sapwood resources. Benchtop experiments in natural and artificial media supported the hypothesis of competition between Ips and Sirex fungal associates, with faster growth and competitive dominance of the bluestain fungus under most scenarios tested. Altogether, this study provides evidence for multiple mechanisms of biotic resistance, whereby a resident community reduces survival or performance of both an invasive insect and its fungal mutualist.

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