Kimberly F. Wallin

Interactions among conifer terpenoids and bark beetles across multiple levels of scale: An attempt to understand links between population patterns and physiological processes

Introduction 80 Bark Beetles and Associated Microorganisms in Host Conifers 80 Localized Reactions: Constitutive and Induced Defenses 83 Whole Trees: Individual Tree Defenses and Group Colonization 85 Populationand LandscapeLevel Dynamics: Bimodal Equilibria, Allee Effects, and Extended Phenotypes 89 Constraints on Population Eruptions 99 How to Link the Scales? 107

FEEDBACK BETWEEN INDIVIDUAL HOST SELECTION BEHAVIOR AND POPULATION DYNAMICS IN AN ERUPTIVE HERBIVORE

We examined the role of population density in host selection behavior of an eruptive insect herbivore, the spruce beetle Dendroctonus rufipennis. We conducted field and laboratory experiments on spruce beetles from 29 endemic and eruptive populations in Alaska and Utah, USA, and Yukon, Canada. Beetles from both population phases colonized trees that had been felled to remove host defenses. However, only beetles from eruptive populations colonized defended, healthy trees. A series of laboratory assays using host-based media amended with varying concentrations of phytochemicals identified several factors affecting population-dependent responses to hosts. First, beetles were repelled by high concentrations of the predominant spruce monoterpene, alpha-pinene, but intermediate concentrations elicited entry and gallery construction. Second, heritability assays suggested high genetic variance of host selection behavior within populations, and between-population differences persisted following rearing in a common environment. Third, beetles from eruptive populations were less likely to enter medium amended with phytochemicals and constructed shorter galleries, which disagreed with our prediction and seemingly contradicted the field observations. However, fourth, beetle avoidance of high concentrations of alpha-pinene decreased with the addition of other beetles, and this effect was more pronounced among beetles from eruptive populations than among those from endemic populations. This interaction broadened the host range of eruptive beetles. We propose that such density-dependent behaviors can maintain heterogeneity among population phases and contribute to positive feedback in herbivore population dynamics. A conceptual model suggests how heritable and environmentally induced variation in host selection behavior can affect bimodal equilibria and numerical thresholds in eruptive species.

Influences of Host Chemicals and Internal Physiology on the Multiple Steps of Postlanding Host Acceptance Behavior of Ips pini (Coleoptera: Scolytidae)

Abstract A series of bioassays were performed to evaluate the effects of host tree monoterpenes on initial entry, within-tissue orientation, and gallery construction by the bark beetle Ips pini (Say). Monoterpenes at concentrations present in host trees affected all stages of postlanding host acceptance behavior. However, the effects of each monoterpene varied with the particular stage of the orientation sequence. The number of beetles entering a phloem-based medium decreased with increased concentrations of most monoterpenes. An exception occurred with β-pinene, which elicited increased beetle entry at moderate concentrations. Once beetles began to form galleries within phloem-based media, higher monoterpene concentrations increased the likelihood that they would move from amended to nonamended sections of the substrate. However, low to moderate concentrations of β-pinene arrested beetles within treated regions of the arena. The total gallery length generally decreased with increasing monoterpene concentrations. However, gallery lengths were consistently higher at intermediate concentrations of α-pinene. The enantiomeric composition of ∂-pinene did not influence entrance or gallery formation by I. pini. Moreover, the concentration of monoterpenes appears to be more important than the type of monoterpene in affecting postlanding host selection behavior. There was a positive correlation between host entry and total percentage of lipids within beetles. We describe a new bioassay that evaluates initial host entry by bark beetles, a critical qualitative decision in their life history, and relates this decision to quantitative aspects of host chemistry. Our results indicate that postlanding host acceptance is a multistep process shaped by environmental conditions and internal physiological state of the insect.

EFFECTS OF FOLIVORY ON SUBCORTICAL PLANT DEFENSES: CAN DEFENSE THEORIES PREDICT INTERGUILD PROCESSES?

The manner and extent to which physiological alterations resulting from folivory can affect the growth, survival, and resistance of trees against subsequent insects and fungi is poorly understood. Information obtained under natural conditions and with subcortically feeding insects is particularly lacking. We evaluated the effects of varying levels of natural feeding by a folivore on subsequent host growth, survival, and suitability to subcortical insects and fungi and also considered implications as to how source limitations caused by defoliation relate to current plant defense theories. The study system consisted of Choristoneura pinus pinus, the jack pine budworm, on Pinus banksiana Lamb., jack pine. We quantified a range of defoliation by C. pinus pinus in test trees and measured parameters of host defenses and colonization by bark beetles (Coleoptera: Scolytidae) and woodborers (Coleoptera: Cerambycidae). We also measured colonization and accompanying tree mortality attributable to these insects. Tree physiological parameters and insect colonization patterns were measured over a 24-mo period. Primary resin flow rates and the ability of active responses to confine the bark beetles fungal symbiont Ophiostoma ips within the phloem, were reduced by high levels of defoliation. These patterns were further influenced by host seasonal phenology and time since defoliation. The predominant subcortical insects responding to defoliation by C. pinus pinus were Ips grandicollis and Monochamus carolinensis. Colonization by these insects together increased exponentially in relation to defoliation level, but the two species differentially exploited trees from particular defoliation levels. The loss of growth among surviving trees increased with defoliation intensity. However, growth and defensive capacity were not related, either negatively or positively, during any interval of this study. Depending on the length of time since defoliation stress, the relationship between plant defense and defoliation intensity was either parabolic, as predicted by growth differentiation theory, or inverse linear, as predicted by plant stress theory. Thus, differing models depicting how carbon allocation and overall carbon availability can influence secondary-chemical metabolism in plants may represent various stages along a temporal continuum. Our results suggest that the time since a stress is exerted is an important variant that should be incorporated into synthetic theories of plant defense. These results also suggest that integrative models of plant defense theory can be extended to describe impacts on community-level interactions.

Altered Constitutive and Inducible Phloem Monoterpenes Following Natural Defoliation of Jack Pine: Implications to Host Mediated Interguild Interactions and Plant Defense Theories

Foliar feeding by the jack pine budworm Choristoneura pinus pinus altered the constitutive and induced monoterpene content and composition of Pinus banksiana phloem. In constitutive phloem tissue the ratios of α-pinene to β-pinene decreased with defoliation intensity. Biochemical responses to simulated bark beetle attack were also influenced by defoliation intensity. Total monoterpene concentrations were always higher in induced than constitutive tissue, but the extent and rate of monoterpene accumulation, and also proportionate changes in monoterpenes during induction, varied with defoliation intensity. Quantitative and compositional changes in response to simulated bark beetle attack were also affected by host seasonal phenology and time since defoliation. There was a positive relationship between myrcene concentration and arrival by the bark beetle Ips grandicollis. Bark beetle arrival rates were more strongly associated with the chemical composition of constitutive than reaction phloem chemistry. However, chemical changes during induced host responses were also associated with beetle behavior. The ratio of α-pinene to β-pinene during the first three days of induction was consistently associated with both defoliation by C. pinus pinus and susceptibility to I. grandicollis. These results show that direct injury to one plant tissue, foliage, cannot only cause chemical changes in another tissue, phloem, but such changes can be greater in the tissue not directly affected. The influence of defoliation intensity on monoterpene accumulation suggests a link between production and allocation of carbon within P. banksiana. The relationship between defoliation level and induced monoterpene concentrations was either parabolic or inverse, depending on the interval following defoliation. Likewise, the relationship between plant growth and defoliation intensity varied with the length of time following defoliation. Thus, plant defense theories can be improved by incorporating the length of time during which the effects of a stress are exerted.

Phylogeography of spruce beetles (Dendroctonus rufipennis Kirby) (Curculionidae: Scolytinae) in North America

Tree‐feeding insects that are widespread in north temperate regions are excellent models for studying how past glaciations have impacted differentiation and speciation. We used mitochondrial DNA (mtDNA) sequences and allele frequencies at nine microsatellite loci to examine genetic population structure across the current range of the spruce beetle (Dendroctonus rufipennis), an economically important insect in North America. Two major haplotype groups occur across northern North America, from Newfoundland to Alaska, on white spruce (Picea glauca), and a third distinctive haplotype group occurs throughout the Rocky Mountains on Engelmann spruce (Picea engelmannii). The two mtDNA lineages found in northern populations are 3–4% divergent from each other and from the lineages found in the Rocky Mountains. Analyses of microsatellite data also suggest the existence of major population groupings associated with different geographical regions. In the Pacific Northwest, concordant contact zones for genetically distinct populations of spruce beetles and their principal hosts appear to reflect recent secondary contact. Although we could detect no evidence of historical mtDNA gene flow between allopatric population groups, patterns of variation in the Pacific Northwest suggest recent hybridization and introgression. Together with the pollen record for spruce, they also suggest that beetles have spread from at least three glacial refugia. A minimum estimate of divergence time between the Rocky Mountain and northern populations was 1.7 Myr (million years), presumably reflecting the combined effects of isolation during multiple glacial cycles.

Seasonality and Lure Preference of Bark Beetles (Curculionidae: Scolytinae) and Associates in a Northern Arizona Ponderosa Pine Forest

Abstract Ponderosa pine forests in northern Arizona have historically experienced limited bark beetle-caused tree mortality, and little is known about the bark beetle community in these forests. Our objectives were to describe the flight seasonality and lure preference of bark beetles and their associates in these forests. We monitored bark beetle populations for 24 consecutive months in 2002 and 2003 using Lindgren funnel traps with five different pheromone lures. In both years, the majority of bark beetles were trapped between May and October, and the peak captures of coleopteran predator species, Enoclerus (F.) (Cleridae) and Temnochila chlorodia (Mannerheim), occurred between June and August. Trap catches of Elacatis (Coleoptera: Othniidae, now Salpingidae), a suspected predator, peaked early in the spring. For wood borers, trap catches of the Buprestidae family peaked in late May/early June, and catches of the Cerambycidae family peaked in July/August. The lure targeted for Dendroctonus brevicomis LeConte attracted the largest percentage of all Dendroctonus beetles except for D. valens LeConte, which was attracted in highest percentage to the lure targeted for D. valens. The lure targeted for Ips pini attracted the highest percentage of beetles for all three Ips species [I.pini (Say), I. latidens (LeConte), and I. lecontei Swaine] and the two predators, Enoclerus and T. chlorodia. The lures targeted for D. valens and I. pini attracted the highest percentage of beetles in the Elacatis genus and the Cerambycidae family. Beetles in the Buprestidae family showed no strong preference for any lure type.

Seasonal dynamics of tree growth, physiology, and resin defenses in a northern Arizona ponderosa pine forest

During periods of resource stress, such as drought, allocating limited photosynthate between growth and defense is a crucial component of tree survival. Our objectives were to describe the seasonal dynamics of physiology, growth, and resin defense of southwestern ponderosa pine (Pinus ponderosa Dougl. ex P. & C. Laws.) which undergoes regular seasonal drought. We measured leaf-level net photosynthetic rate, leaf water potential, resin flow after phloem wounding, and growth in 24 consecutive months in 2002 and 2003. Precipitation was below average in both years, and 2002 was an extreme drought. In both years, the highest resin flow occurred when tree water stress was highest and photosynthesis was low. Belowground growth was highest in August in both years. Aboveground growth occurred primarily between May and August and was greater in 2003 than in 2002. Temporal variation in resin flow was positively related to temporal variation in needle and radial growth but was not related to temporal variation in roo...

Density‐mediated responses of bark beetles to host allelochemicals: a link between individual behaviour and population dynamics

Abstract  1. Bark beetles (Coleoptera: Scolytidae) accept or reject host conifers based partly on concentrations of phloem monoterpenes. They colonise trees in aggregations, in response to pheromones that attract flying beetles to trees undergoing colonisation. A series of entry and gallery construction assays was conducted to determine whether responses by individual beetles to monoterpenes are altered by pheromones and/or the presence of other beetles.

Heritability of Host Acceptance and Gallery Construction Behaviors of the Bark Beetle Ips pini (Coleoptera: Scolytidae)

Abstract We examined genetic variation in host selection behavior of a phloeophagous insect herbivore. Data from paternal families of the bark beetle Ips pini (Say) were used to estimate the heritability of host acceptance and gallery construction behaviors. Males are the host-selecting gender in this genus. Male beetles were assayed over three generations to determine whether they rejected or accepted host media amended with concentrations of alpha-pinene that simulated host tissue, and 10% from each group were selected for breeding lines. In a separate experiment, 10% of individuals constructing the shortest and 10% of individuals constructing the longest galleries in this medium were established in separate breeding lines. The results indicate high additive genetic variation with respect to both traits. On the basis of the results with full-sib breeding lines, we estimated heritability of host acceptance behavior (i.e., entry into simulated hosts) at 0.78 and heritability of gallery construction behavior at 0.64. The divergence between lines in host acceptance and gallery construction behaviors was associated with paternal performance and was symmetrical. This study demonstrates that the use of phytochemical cues to accept potential hosts has a heritable component in bark beetles. I. pini is a useful and convenient model for such studies.