Nitrogen budgets of phloem-feeding bark beetles with and without symbiotic fungi

The nitrogen content of plant tissue is low relative to that of herbivores; as a consequence, dietary N can limit the growth and reproduction of herbivores and select for attributes that increase N acquisition. Bark beetles face a particularly severe challenge because the phloem that they consume is very low in nitrogen and phosphorus relative to their requirements. We quantified variation in the phloem concentrations of N and P in the host tree, Pinus taeda, and evaluated the following hypotheses regarding the role of sym- biotic fungi in nutrient budgets of the herbivore Dendroctonus frontalis: D. frontalis ex- perience variation in phloem nutrient concentrations across several spatial scales (HI); mycangial fungi enhance the diet of D. frontalis larvae by contributing to the acquisition of N and P (H2); Ophiostoma minus, an apparently antagonistic fungal symbiont, hinders D. frontalis larvae because it does not enhance nutrient concentrations of the phloem as much as mycangial fungi do (H3); and larvae of bark beetle species that lack mycangial fungi must consume more phloem to accomplish the same growth as larvae of D. frontalis (H4). In addition, we developed a general model for the N budgets of herbivorous insects that identifies the possible combinations of dietary and physiological parameters that can allow developmental success on low-nutrient diets. Spatial variation in phloem N was mostly at the level of trees within sites (a scale of meters) while P mostly varied among sites (a scale of kilometers). Trees with higher N content produced larger D. frontalis adults. Prior to infestation by beetles, phloem nutrient concentrations were very uniform within trees and very low relative to that of the bark beetles (N and P concentrations of D. frontalis adults were 28 and 8 times greater, re- spectively). During infestation, phloem nutrient concentrations increased overall and be- came highly variable within trees. Nitrogen concentrations increased from 0.40 + 0.01% (mean + 1 SE) in uninfested phloem to 0.86 + 0.03% in the phloem surrounding successfully developing D. frontalis larvae, which are typically associated with one or two species of mutualistic mycangial fungi. Nitrogen concentrations were intermediate in other micro- habitats within infested trees, including regions with no adult colonization, with failed larval development, or colonized by the antagonistic bluestain fungus 0. minus. We pa- rameterized a general nutrient-budget model for D. frontalis and a sympatric non-mycangial bark beetle, Ips grandicollis, which indicated that (1) mycangial fungi provide their benefits by concentrating dietary N for larvae; (2) 0. minus may exert its antagonistic effects on D. frontalis larvae by failing to concentrate dietary N as much as mycangial fungi do; (3) non-mycangial bark beetles meet their N budgets through high consumption of unaltered, low-N phloem; and (4) larvae should easily meet their P requirements with any combination of consumption rate and development time that allows them to meet their N requirements. Alternative strategies for N acquisition may have general consequences for the population dynamics and community interactions of bark beetles.