Nadir Erbilgin

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

Exogenous application of methyl jasmonate elicits defenses in Norway spruce (Picea abies) and reduces host colonization by the bark beetle Ips typographus

The terpenoid and phenolic constituents of conifers have been implicated in protecting trees from infestation by bark beetles and phytopathogenic fungi, but it has been difficult to prove these defensive roles under natural conditions. We used methyl jasmonate, a well-known inducer of plant defense responses, to manipulate the biochemistry and anatomy of mature Picea abies (Norway spruce) trees and to test their resistance to attack by Ips typographus (the spruce bark beetle). Bark sections of P. abies treated with methyl jasmonate had significantly less I. typographus colonization than bark sections in the controls and exhibited shorter parental galleries and fewer eggs had been deposited. The numbers of beetles that emerged and mean dry weight per beetle were also significantly lower in methyl jasmonate-treated bark. In addition, fewer beetles were attracted to conspecifics tunneling in methyl jasmonate-treated bark. Stem sections of P. abies treated with methyl jasmonate had an increased number of traumatic resin ducts and a higher concentration of terpenes than untreated sections, whereas the concentration of soluble phenolics did not differ between treatments. The increased amount of terpenoid resin present in methyl jasmonate-treated bark could be directly responsible for the observed decrease in I. typographus colonization and reproduction.

Mountain Pine Beetles Colonizing Historical and Naïve Host Trees Are Associated with a Bacterial Community Highly Enriched in Genes Contributing to Terpene Metabolism

ABSTRACT The mountain pine beetle, Dendroctonus ponderosae, is a subcortical herbivore native to western North America that can kill healthy conifers by overcoming host tree defenses, which consist largely of high terpene concentrations. The mechanisms by which these beetles contend with toxic compounds are not well understood. Here, we explore a component of the hypothesis that beetle-associated bacterial symbionts contribute to the ability of D. ponderosae to overcome tree defenses by assisting with terpene detoxification. Such symbionts may facilitate host tree transitions during range expansions currently being driven by climate change. For example, this insect has recently breached the historical geophysical barrier of the Canadian Rocky Mountains, providing access to näive tree hosts and unprecedented connectivity to eastern forests. We use culture-independent techniques to describe the bacterial community associated with D. ponderosae beetles and their galleries from their historical host, Pinus contorta, and their more recent host, hybrid P. contorta-Pinus banksiana. We show that these communities are enriched with genes involved in terpene degradation compared with other plant biomass-processing microbial communities. These pine beetle microbial communities are dominated by members of the genera Pseudomonas, Rahnella, Serratia, and Burkholderia, and the majority of genes involved in terpene degradation belong to these genera. Our work provides the first metagenome of bacterial communities associated with a bark beetle and is consistent with a potential microbial contribution to detoxification of tree defenses needed to survive the subcortical environment.

Effect of varying monoterpene concentrations on the response of Ips pini (Coleoptera: Scolytidae) to its aggregation pheromone: implications for pest management and ecology of bark beetles

Abstract  1 Host plant terpenes can influence attraction of conifer bark beetles to their aggregation pheromones: both synergistic and inhibitory compounds have been reported. However, we know little about how varying concentrations of individual monoterpenes affect responses.

Population dynamics in changing environments: the case of an eruptive forest pest species.

In recent decades we have seen rapid and co‐occurring changes in landscape structure, species distributions and even climate as consequences of human activity. Such changes affect the dynamics of the interaction between major forest pest species, such as bark beetles (Coleoptera: Curculionidae, Scolytinae), and their host trees. Normally breeding mostly in broken or severely stressed spruce; at high population densities some bark beetle species can colonise and kill healthy trees on scales ranging from single trees in a stand to multi‐annual landscape‐wide outbreaks. In Eurasia, the largest outbreaks are caused by the spruce bark beetle, Ips typographus (Linnaeus), which is common and shares a wide distribution with its main host, Norway spruce (Picea abies Karst.). A large literature is now available, from which this review aims to synthesize research relevant for the population dynamics of I. typographus and co‐occurring species under changing conditions.

Chemical similarity between historical and novel host plants promotes range and host expansion of the mountain pine beetle in a naïve host ecosystem

Host plant secondary chemistry can have cascading impacts on host and range expansion of herbivorous insect populations. We investigated the role of host secondary compounds on pheromone production by the mountain pine beetle (Dendroctonus ponderosae) (MPB) and beetle attraction in response to a historical (lodgepole pine, Pinus contorta var. latifolia) and a novel (jack pine, Pinus banksiana) hosts, as pheromones regulate the host colonization process. Beetles emit the same pheromones from both hosts, but more trans-verbenol, the primary aggregation pheromone, was emitted by female beetles on the novel host. The phloem of the novel host contains more α-pinene, a secondary compound that is the precursor for trans-verbenol production in beetle, than the historical host. Beetle-induced emission of 3-carene, another secondary compound found in both hosts, was also higher from the novel host. Field tests showed that the addition of 3-carene to the pheromone mixture mimicking the aggregation pheromones produced from the two host species increased beetle capture. We conclude that chemical similarity between historical and novel hosts has facilitated host expansion of MPB in jack pine forests through the exploitation of common host secondary compounds for pheromone production and aggregation on the hosts. Furthermore, broods emerging from the novel host were larger in terms of body size.

Association of declining red pine stands with reduced populations of bark beetle predators, seasonal increases in root colonizing insects, and incidence of root pathogens

Abstract Declining red pine, Pinus resinosa (Aitman), stands in the Great Lakes region appear to arise from a complex of biotic and abiotic factors. We monitored stem and root colonizing beetles in declining and healthy plantations in Wisconsin from 1997 to 1999. We also conducted systematic field excavations and laboratory isolations of various root pathogens. Multiple funnel traps were baited with the synthetic aggregation pheromones of the two most common bark beetle (Coleoptera: Scolytidae) species in the region, Ips pini (Say) and Ips grandicollis (Eichhoff). Lower-stem flight traps were baited with 1:1 (+)-α-pinene:75% ethanol, and pitfall traps were baited with 1:1 (−)-α-pinene:75% ethanol. Healthy stands had higher populations of predators, particularly Thanasimus dubius (F.) (Coleoptera: Cleridae), Platysoma cylindrica (Paykull) (Coleoptera: Histeridae), and Platysoma parallelum Say than declining stands. Seasonal abundance patterns of predators and Ips also varied between declining and healthy stands. Declining stands had higher numbers of Ips and lower numbers of predators early in the season, whereas healthy stands had higher predator populations in the early season. Declining stands had more lower stem infesting bark beetles Dendroctonus valens LeConte (Scolytidae) and weevils (Curculionidae) Pissodes spp. Surprisingly, healthy stands had more root weevils, Hylobius pales (Herbst) and Hylobius radicis Buchanan, and root bark beetle Hylastes porculus Erichson, over the entire season. However, spatial by temporal patterns again were important. Populations of root colonizing insects were higher in healthy stands early in the season, but higher in declining stands throughout much of the ovipositional period. These results suggest dispersal patterns and overwintering behaviors are important in the interactions among herbivores, predators, and host plant condition in Red Pine Decline. The principal fungi isolated from roots were Leptographium procerum (Kendr.) Wingfield and Leptographium terebrantis Barras & Perry. These were more prevalent in declining than healthy stands. Staining fungi were more frequently isolated from roots of trees at the pocket margin than from trees in the asymptomatic portion of declining stands. Heterobasidion annosum (Fr.) Bref. was not isolated from root samples or stem disks, despite 40% recovery in positive controls using the latter method. Likewise, Armillaria spp. were not associated with declining plantations. Our results further support the view that forest declines are due to complex interactions among multiple biotic and abiotic stresses, and exhibit particular spatial and temporal patterns.

Response to host volatiles by native and introduced populations of Dendroctonus valens (Coleoptera: Curculionidae, Scolytinae) in North America and China

Bark beetles (Coleoptera: Curculionidae, Scolytinae) have specialized feeding habits, and commonly colonize only one or a few closely related host genera in their geographical ranges. The red turpentine beetle, Dendroctonus valens LeConte, has a broad geographic distribution in North America and exploits volatile cues from a wide variety of pines in selecting hosts. Semiochemicals have been investigated for D. valens in North America and in its introduced range in China, yielding apparent regional differences in response to various host volatiles. Testing volatiles as attractants for D. valens in its native and introduced ranges provides an opportunity to determine whether geographic separation promotes local adaptation to host compounds and to explore potential behavioral divergence in native and introduced regions. Furthermore, understanding the chemical ecology of host selection facilitates development of semiochemicals for monitoring and controlling bark beetles, especially during the process of expansion into new geographic ranges. We investigated the responses of D. valens to various monoterpenes across a wide range of sites across North America and one site in China, and used the resulting information to develop an optimal lure for monitoring populations of D. valens throughout its Holarctic range. Semiochemicals were selected based on previous work with D. valens: (R)-(+)-α-pinene, (S)-(−)-α-pinene, (S)-(−)-β-pinene, (S)-(+)-3-carene, a commercially available lure [1:1:1 ratio of (R)-(+)-α-pinene:(S)-(−)-β-pinene:(S)-(+)-3-carene], and a blank control. At the release rates used, (+)-3-carene was the most attractive monoterpene tested throughout the native range in North America and introduced range in China, confirming results from Chinese studies. In addition to reporting a more effective lure for D. valens, we present a straightforward statistical procedure for analysis of insect trap count data yielding cells with zero counts, an outcome that is common but makes the estimation of the variance with a Generalized Linear Model unreliable because of the variability/mean count dependency.

Population Dynamics of Ips pini and Ips grandicollis in Red Pine Plantations in Wisconsin: Within- and Between-Year Associations with Predators, Competitors, and Habitat Quality

Abstract We sampled bark beetle (Coleoptera: Scolytidae) populations in 17 declining and healthy red pine plantations in Wisconsin over 3 yr. We tested for potential relationships among numbers of bark beetles, conspecifics and competitors, and predators within and among flight seasons to help identify factors affecting population densities. The two most common bark beetle species obtained were Ips pini (Say) and Ips grandicollis (Eichhoff). The predominant predators obtained were Thanasimus dubius (F.) (Cleridae), Platysoma cylindrica (Paykull) (Histeridae), and Platysoma parallelum Say. Declining stands contained significantly more Ips than did healthy stands during the early portion of the season. Healthy stands had more predators than declining stands. There were strong delayed inverse relationships between I. pini and predators at the site level, both within and between flight seasons. The number of I. pini caught during the late portion of the season was lower when each of the above predators was more abundant earlier in the season, during both 1998 and 1999. Likewise, numbers of I. pini and I. grandicollis caught during the early portion of the year were inversely related to numbers of predators caught during the previous year. Although Ips trap counts showed significant correlations with each predator species, simple predator-prey models did not necessarily improve fits based on habitat quality (i.e., Ips numbers regressed on prior Ips numbers). We did not observe evidence for interspecific competition among Ips spp. This pattern is consistent with the view that host plant quality and predation jointly affect I. pini and I. grandicollis population dynamics. These results emphasize the importance of interactions among host tree physiology, predation, and dispersal in the population dynamics of phloeophagous herbivores, and have implications to forest management.

Effects of host tree species on attractiveness of tunneling pine engravers, Ips pini, to conspecifics and insect predators.

The effect of host tree species on the attractiveness of tunneling Ips pini to flying beetles and their insect predators in Wisconsin was investigated. Tree species influenced the flight response of both predators and prey in the same rank order. Ips pini and its major predators, Thanasimus dubius and Platysoma cylindrica, were more attracted to I. pini males boring into bark–phloem disks of Pinus strobus L. than Pinus banksiana Lamb, and least attracted to I. pini males boring into bark–phloem disks of Pinus resinosa. Sources of within-tree, between-tree, and between-species variation in the degree of attraction elicited by tunneling beetles were quantified. A bioassay for evaluating host tree effects on pheromone based communication among bark beetles under conditions of controlled beetle entry was developed. Possible mechanisms of host species effects on the dynamics of predator and prey interactions in bark beetle ecology are discussed.