Allan Carroll

In mutualisms with bark beetles (Coleoptera: Curculionidae; Scolytinae), fungi benefit from dispersal to new habitats while granting their insect vectors access to resources via their phytopathogenic activities and supplementation of beetle nutrition. Alniphagus aspericollis, the alder bark beetle, is a bole-infesting beetle that kills red alder, Alnus rubra, a nitrogen-fixing hardwood native to the Pacific Coast of North America. Unlike most tree-killing bark beetles, the alder bark beetle is not regularly associated with ophiostomatoid fungi (Ophiostomatales and Microascales), but is instead associated with a previously undescribed species of Neonectria fungus (Hypocreales). I hypothesized that the alder bark beetle–Neonectria sp. nov. association represents a unique bark beetle–fungus mutualism that is similar to bark beetle–ophiostomatoid mutualisms in conifers. I first characterized the branch-overwintering component of the alder bark beetle life cycle, described Neonectria sp. nov. as Neonectria bordenii sp. nov., and developed a qPCR assay to enable detection of N. bordenii from alder bark beetle DNA. I then evaluated the following predictions, at five sites throughout southwestern British Columbia, Canada: (1) the alder bark beetle vectors N. bordenii; and (2) the beetle uses both an aggregation pheromone and N. bordenii to facilitate spatially-clustered mass-attacks on red alders. I tested prediction (1) according to Leach’s postulates, using qPCR and culturing methods to reveal that N. bordenii was present on emergent alder bark beetles at frequencies consistent with established bark beetle–fungus mutualisms, and that attacking beetles transmitted N. bordenii into red alders. To test prediction (2), I quantified patterns of host colonization by alder bark beetles in one-hectare plots, demonstrating spatial clustering of attacks on trees that supports the existence of an alder bark beetle aggregation pheromone. Previously attacked trees were more likely to be attacked and produced more offspring than previously unaffected trees, suggesting a mutualistic function of N. bordenii. Potentially high rates of alder bark beetle population increase were observed, raising concerns of widespread red alder decline. My research provides valuable insights into the evolution of bark beetle–fungus mutualisms by expanding upon known associations to include a hardwood-killing bark beetle and its unique putative mutualist.

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Favorable climatic conditions at historical range boundaries have allowed several insect specieswith eruptive population dynamics to invade adjacent habitats, sometimes causing severe impacts on forest health. However, the potential for recurrent outbreaks in novel habitats is uncertain because the reproductive fitness exhibited during outbreaks is temporary. Persistence in recently invaded habitats depends on the ability of the invasive species to persist at sub-outbreak or endemic population densities.I investigated the potential for mountain pine beetle (Dendroctonus ponderosae) to persist in its expanded outbreak range by quantifying interactions that are critical for survival of endemic populations. In lodgepole pine (Pinus contorta var. latifolia), epidemic-phase mountain pine beetles (hereafter ‘epidemic-phase beetles’) attack vigorous trees and endemic populations (hereafter ‘endemic-phase beetles’) preferentially colonize moribund trees. Although endemic- phase beetles exhibited this behavior in both habitats, the endemic niche in lodgepole pine was much more suitable than in jack pine (Pinus banksiana) habitats. Endemic susceptible trees were scarce in jack pine as compared to lodgepole pine stands (1-5/ha vs 6-13/ha, respectively), and susceptible host abundance was correlated with stand density index (SDI), a measure ofinter-tree competition. Endemic susceptible jack pines were commonly occupied by woodboring beetles (Cerambycidae and Buprestidae), 25-60% of trees in a stand, and dissected bolts harvested from such trees exhibited high phloem consumption, mean = 58%, compared to trees occupied solely by secondary bark beetles, mean = 3%. I further showed that woodborer larvaeattracted woodpeckers to forage on endemic susceptible trees, suggesting that woodpeckers ininvaded habitats may have stronger impacts on the survival of endemic-phase beetles comparedto the native range.I show that: 1) mountain pine beetles can differentiate between vigorous and defensivelycompromised trees in lodgepole and jack pine stands, 2) jack pine habitats are resource poor and have elevated competition for phloem compared to lodgepole pine habitats, and 3) niche overlap with woodborers in jack pine increases the risk of mortality by woodpeckers adapted to exploiting woodborers as food. Due to the reduced endemic niche, post-epidemic populations are unlikely to persist in sufficient densities to facilitate future eruptions in western boreal jack pine forests.

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Global climate change is affecting species from all taxonomic groups. Their response to warming and precipitation trends is highly variable, and will likely lead to changes in ecosystem composition that may affect resilience and stability. Eruptive forest insects compete directly with humans for forest resources, and the distribution and magnitude of epidemics is increasing. Here, I describe a series of manipulative experiments using the mountain pine beetle (Dendroctonus ponderosae) system to examine biological and life history traits of both the beetle and hosts as they pertain to eruptive population dynamics and range expansion in a warming environment. Mountain pine beetle exhibits population phase-dependent host selection behavior, which I demonstrated is informed directly by monoterpene volatiles in host resin, and reinforced by context-dependent maternal effects arising from parental experience. Recently, mountain pine beetles have experienced dramatic range expansion into novel montane and boreal forests of western Canada. Depressed defensive capability of trees in novel forests may increase generation survival of beetle populations, potentially exacerbating outbreaks in novel systems, and enhance positive feedbacks associated with epidemic phases. Of particular concern is the tendency for elevated levels of α-pinene, an aggregation pheromone precursor, in the defensive resin of trees in novel habitats. I demonstrated that the qualitative content of monoterpenes, specifically the relative concentration of (+)- and (-)-α-pinene, influences the ability of the beetle to aggregate and mass-attack healthy hosts, and may exacerbate outbreaks on a landscape scale, thereby potentially increasing the rate of spread of beetles in novel forests. Finally, I demonstrated that the close association of mountain pine beetle with the defensive expression of hosts has led to selection in native forests for enhanced defenses, and a lack of coevolution in novel forests has likely led to the increased susceptibility to mortality. The present study has advanced our knowledge of eruptive insect dynamics and the response of these economically important species to climate change. This thesis contributes to the body of knowledge pertaining to ecological theory of population dynamics and invasion biology, and identifies areas for further study and effort to mitigate the biological consequences of anthropogenic modification to the environment.

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