Nitrogen Budgets of Phloem-Feeding Bark Beetles With and Without Symbiotic Fungi

Abstract

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 symbiotic fungi in nutrient budgets of the herbivore Dendroctonus frontalis: D. frontalis experience variation in phloem nutrient concentrations across several spatial scales (H1); 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, respectively). During infestation, phloem nutrient concentrations increased overall and became 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 microhabitats within infested trees, including regions with no adult colonization, with failed larval development, or colonized by the antagonistic bluestain fungus O. minus. We parameterized 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) O. 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. A...

La stimulation des défenses de l’arbre par les champignons Ophiostomatoïdes peut expliquer le succès des attaques de Scolytes sur conifères

“…Considering the near-obligate and facultative parasitic species, it is thought that fungi can improve larval diet through modifying the substrate or providing complementary nutrients such as vitamins, proteins or sterols Six, 2003). Evidence for a role of mycangial basidiomycetes in helping D. frontalis to meet its nitrogen needs has been found (Ayres et al, 2000). Similarly, the presence of the Ophiostomatoid species Grosmannia clavigera and Ophiostoma montium can increase the nitrogen levels in the phloem of trees attacked by D. ponderosae by 40%, probably through their ability to restitute nitrogen from the sapwood to the phloem (Bleiker and Six, 2007), and all larval stages and the adults of the insect can feed on the fungi (Adams and .…”

Anthropogenic effects on interaction outcomes: examples from insect-microbial symbioses in forest and savanna ecosystems

“…Bark beetles have evolved two strategies for contending with this problem. Some construct long feeding galleries and consume large amounts of phloem relative to their final adult size (Ayres et al 2000). These species do not appear to gain benefit from feeding on fungi and the fungi they carry are not highly specific.…”

Destructive Tree Diseases Associated with Ambrosia and Bark Beetles: Black Swan Events in Tree Pathology?

“…(Fig. 5H) (6,12,79,99,122,150) (Table 1). For example, fungi that were associated with C. columbianus activity on silver maple (Acer saccharinum) caused no significant damage on detached or intact host material when used in inoculation experiments (79).…”

“…And for some of the bark beetles, fungal symbionts provide sterols, nitrogen and other nutrients that are required for, or facilitate, development and reproduction (1,12,19,20).…”

“…Some reversion to conifer hosts occurred, but most extant ambrosia beetles are found in angiosperms. Extant bark beetles are also most common on angiosperms, although the most economically important species occur on pines.Bark beetles feed on host phloem, but many species supplement their diets with symbiotic fungi (12,20,146). In contrast, most ambrosia beetles subsist entirely on fungi (14,15,17,144).…”