W2187: Interactions of emerging threats and bark beetle-microbial dynamics in forest ecosystems

(Multistate Research Project)

Status: Inactive/Terminating

Project Menu

W2187: Interactions of emerging threats and bark beetle-microbial dynamics in forest ecosystems

Duration: 10/01/2009 to 09/30/2014

Administrative Advisor(s):


NIFA Reps:


Non-Technical Summary

Statement of Issues and Justification

The need, as indicated by stakeholders:

A changing set of factors is influencing western forests at a scale that some argue is unprecedented in the modern era. Much of the Western US has experienced drought for the past 10 years. Changing climate has increased mean summer and winter temperatures, as well as mean low temperatures, above those in recorded history. Invasive exotic species have altered the species composition of landscapes. These are just a few of the factors altering forest susceptibility to insects and pathogens. These effects cascade, as, for example, insects and pathogens alter fire regimes, and with increased temperature and drought, they facilitate an increase in the number, size and severity of forest fires. Even the public in western states is well aware of these issues.

Changes in land use patterns are contributing to intensification of interactions at the forest - human interface, which imposes societal goals on natural ecosystems. Among the demands citizens expect from forested ecosystems are resistance to fire, carbon sequestration, clean water and aesthetic quality. Even natural forest succession is perceived by some to be undesirable. Society increasingly demands ecosystem services at a time when these ecosystems are changing rapidly. For example, hardwoods which were often ignored are now becoming important to land managers and the public. In the Intermountain West, land managers have become aware that aspen is a critical species and may be declining. We have little research to guide us in restoration efforts. Sudden oak death is changing the composition of West Coast forests, with unknown consequences. In Midwestern states, the exotic Emerald Ash borer threatens both urban and wild ash; again, we know little about this insect and its microbial associates.

The importance of the work, and the consequences if it is not done:



Understanding dynamics of insect, pathogen and associated microbes in forests is critical to maintaining the ecosystem services forests provide. We have learned that there are natural constraints on pathogen and insect populations, which climate change and succession seem to reduce, causing outbreaks which affect societal goals and require management at a cost to society. These changes are occurring at scales beyond our experience, not only at the state level, but at regional and even international scales. Yet, numbers of entomologists and pathologists are at an all time low. Funding for both basic and applied research has also declined. We must work collectively to address the problems facing forests today, and to train future professionals so that society does not lose the capacity to respond to new or changing environmental crises.

Our research on interactions among insects and fungi and their diversity is providing conceptual and practical models of how invasive insects and fungi can work to degrade forests. Changing large scale factors are altering forests in ways that we could not predict, and in ways that are negatively impacting society. Without continued and integrated study of forests, these negative impacts will become the norm and they will deprive society of the ecosystem services that forests provide. One need only look at the recent increase in forest fire size and intensity. These changes, so far mostly the result of increasing temperature and drought, have already cost management agencies many times more than their normal fire budgets; today the USDA Forest Service spends 60% of its entire budget on fire control.



Our efforts to characterize insect, fungus and host tree interactions have already provided benefits. We know that some fungi are detrimental to bark beetles, some are beneficial, and some can be either depending on context. Efforts are underway to use fungal population structures as 1) indicators of trends in bark beetle outbreaks; and 2) to manage bark beetle populations. We understand some system specific dynamics and comparison approaches at individual and local scales, but not at cross scale interactions needed to address today's rapidly changing landscape. We have the tools to address many of the questions; we need a collaborative, multistate, and even an international approach to understand feedbacks among insects, microbial associates, the forests that host them, and the agents of change driving this complex system.

The advantages for doing the work as a multistate effort:

Working in a multistate effort has been very productive for this group in the past, and is essential in order to bring together teams with sufficient expertise to address the problems. Our group has been a model for other multi state efforts that integrate insects and pathogens, for example NCR-193. Unfortunately, as we have developed an understanding of one system, the system is changed by factors such as climate change or the introduction of exotic insects and fungi into forests. Addressing these new or changing issues requires a team effort, beyond that which any single institution, or even several individual PI's can amass. Insects and pathogens do not recognize national boundaries and Canadian scientists have expressed interest in participating in this project under their own agency support.

Likely impacts from successfully completing the work:

Our efforts will lead to improved ability to predict the effects of insects and diseases in forests as we enter an era when forests are subjected to changes that we have never seen before. On a practical level, we will learn to recognize key components of pest systems, which will enable us to better predict and monitor the effects of forest insect and disease outbreaks. Key components will also enable us to recognize new infestations of exotic organisms earlier in their establishment, increasing the likelihood that the infestation may be managed or eliminated before extensive and costly management is needed. Through these efforts, we will train multi-disciplinary scientists and professionals to provide necessary information for science based policy.

Related, Current and Previous Work

A CRIS search using "forest and insect or disease" yielded 148 hits; only 6 were related to our efforts and not work of our current members; and most of those projects could be included in our new project because we have expanded our efforts to include hardwoods and insects other than bark beetles. We will invite the scientists identified to join us in the new project.

Bark beetles and pathogens interact as important disturbance agents in North American forests. This statement in and of itself is significant in that we now recognize the importance of the beneficial roles that these organisms play in forested systems.

PROGRESS:

During the past 5 years, we have learned much about interactions among beetles, pathogens and conifers, and increasingly, hardwoods. Rather than reviewing the extensive literature in this field, we identify areas critical to our understanding of these systems, and highlight key findings fundamental to our future research.

1. Fungal and other microbial associates are important drivers of bark beetle population dynamics:

  • Some symbiotic fungi are beneficial to bark beetles. For example, it is clearly established that some symbiotic fungi can be a food base for bark beetles. There is some evidence, but less well established, that some symbiotic fungi may assist bark beetles in overcoming tree defenses (Erbilgin et al 2005, 2008; Storer et al 2004).

  • Some fungal associates are antagonistic to bark beetles. These include both phoretic fungi and opportunistic fungi that invade beetle-killed trees Metabolites of the root pathogen Heterobasidion annosum reduced ingestion of phloem by Ips paraconfusus (McNee et al 2003).

  • Bacterial associates, phoretic mites, and nematodes can mediate interactions between bark beetles and their fungal symbionts (Cardoza et al 2006).

  • Fungal associates of bark beetles produce volatiles that are exploited as attractants for host finding by parasitoids.

  • Population structure of the fungal associates of the Mountain Pine Beetle shows a dynamic and complex situation; microsatellite profiles highlighted distinct routes of spread of the fungus in western Canada and extensive recombination and gene flow within and between species (Hamelin, pers. comm.)

    2. Exotic invasive insects and fungi are associating with native organisms to exacerbate the ecosystem dysfunction caused by the exotic organism.

  • Successful new associations can be formed between insects, both indigenous and exotic, and exotic invasive pathogens. Examples include Pityophthorus setosus and two species of Ips vectoring the exotic pitch canker pathogen Fusarium circinatum into Monterey pine in California. Another example is of native and exotic ambrosia beetles causing structural injury to oak trees infected with invasive Phytophthora ramorum (Storer et al 2004, Erbilgin et al 2008a,b, McPherson et al 2005; McPherson et al 2008). The relationship of the new exotic asian banded elm bark beetle (Scolytus schevyrewi) and the exotic pathogen(Ophiostoma novo-ulmi) responsible for Dutch elm disease was studied under this project (Jacobi et al 2007).
  • In coevolved systems tree defenses play a crucial role in tree resistance. In non-coevolved systems, there may be little resistance, thereby substantially reducing management options. Often times, that is why invasive exotics are highly successful (e.g. emerald ash borer, Phytophthora ramorum). (Bonello et al. 2006; Eyles et al. 2007; Ockels et al. 2007; Rebek et al 2008).
  • Both exotic and native pathogens can induce a state of resistance in trees that can lead to disease remission in individual trees (e.g. pitch canker) (Blodgett et al. 2007; Bonello and Blodgett 2003; Bonello et al. 2001; Bonello et al. 2006; Eyles et al. 2007a), Erbilgin et al 2009; Gordon et al 2001).

    3. Trees respond to insect and fungal attack by producing chemicals that actively inhibit pathogens, bark beetles and associated microbes. These relationships are typically concentration-dependent, and based on multiple chemical classes. These defenses are both constitutive and induced. Defenses are induced both locally and systemically (and cross-induction of resistance between pathogens and insects is possible (Blodgett et al. 2007; Bonello and Blodgett 2003; Bonello et al. 2006; Raffa and Smalley 1995; Wallis et al. 2008).
  • Tree defenses are modulated by environmental variables, for example nutrient and water availability (Barto et al. 2008; Blodgett et al. 2005; Bonello et al. 2006; Eyles et al. 2007a; Kleczewskiet al 2008; Wallis et al. 2008).

  • Tree defenses are important bottom-up regulators of pathogens, bark beetles and associated microbes. However, this regulation is characterized by thresholds that govern transitions between endemic and irruptive bark beetle population phases (Walin and Raffa 2004; Raffa et al 2007).

  • Expression of systemic induced resistance or susceptibility depends on the target organs. (Blodgett et al.2005, 2007; Bonello et al. 2008).

    4. Predisposing factors affect host biology and subsequent insect attack:

  • There is a high degree of association between symptomatic expression of some diseases and bark beetle attack. (Baker and McManus 2007, Kallas et al 2003, Kearns and Jacobi 2005,Kearns and Jacobi 2007, McPherson et al. 2008; Owen et al. 2005).

  • Defoliation, severe drought, root herbivory and disease, competition for resources, and non-lethal injury caused by fire can impair defenses against pathogens and bark beetles (Baker and Wager 2006; Kearns and Jacobi 2007; Klepzig et al 1991; Omdal et al 2004; Wallin and Raffa 2002).

    5. Bark beetles select hosts based on host chemistry; natural enemies can also respond to host chemistry and to chemicals produced by bark (Erbilgin et al 2007).
  • Sudden oak death cankers emit volatiles that attract ambrosia beetles (McPherson et al. 2008)

  • Predators of bark beetles are attracted to bark beetle pheromones (reviewed in Wood 1982). Sometimes this response is even greater than that of the bark beetles to their own pheromone. However, some bark beetles have complex pheromone plumes that potentially mask their communication from predators. This coevolution between bark beetle and predator provides opportunities to improve population monitoring and management. (Aukema and Raffa, 2005, Dahlsten et al 2004, Raffa et al 2007).

  • Biochemical pathways of pheromone synthesis have been characterized in some bark beetles (reviewed in Tillman et al 1999; Seybold and Tittiger 2003).

    6. Climate change is altering traditional interactions among insects, fungi and their hosts:
  • Warmer temperatures reduce winter mortality and shorten generation times of bark beetles and can lead to outbreaks (Aukema et al 2005; Regniere and Bentz, 2007).
  • Higher temperatures have been accompanied by (allowed?) northward expansion and increased frequency of upslope expansion of mountain pine beetle (Logan et al 2003).

  • Temperature influences the composition of the fungal community associated with bark beetles.

    7. Management tools enable us to influence insect, fungi or host populations. We have so far developed:
  • Semiochemical-based tools for monitoring outbreaks of native bark beetles as well as new introductions (Dahlsten et al. 2003, Aukema and Raffa 2005, Erbilgin et al. 2007, Lee et al. 2007).

  • Climate-based predictions for bark beetle outbreaks and symptom-based predictions for sudden oak death epidemics and induced mortality (Garriston et al. 2003, Kelly et al. 2008, McPherson et al. 2005).

  • Spatially explicit models for focused diseases (Baker et al. in prep.; Kallas et al. 2003; Kearns et al. in prep.).

    EMERGING ISSUES: Although we have learned much about bark beetles and diseases in coniferous ecosystems, there is still much to learn. Our emphasis has been at the level of the individual tree, insect, or fungus. We now need to scale up beyond trees and even stands to look at system level responses. We need to broaden our efforts to look beyond conifers, bark beetles, and fungi to hardwoods and other insects and microbes to truly understand system function, performance and services. Only from this broader base can we begin to understand effects of major factors such as climate change, changing fire regimes, exotic species and increased human presence in forests.

    Objectives

    1. Characterize the diversity and interactions among tree hosts, bark beetles, their natural enemies, and associated microbes.
    2. Characterize feedbacks between bark beetle-microbial interactions and forest ecosystem processes.
    3. Integrate and apply knowledge gained from obj. 1 and 2 to forest ecosystems as influenced by emerging issues such as invasive species, global climate change, changing land use patterns and fire regimes, and multiple and conflicting societal demands.

    Methods

    Our methods are based on the current knowledge and expertise of current participants. These efforts will expand as more PI's join in these efforts. Objective 1: Characterize interactions among trees, pathogens, and bark beetles, their natural enemies, and associated microbes. We will examine the nature and the role played by constitutive and induced, local and systemic tree resistance/susceptibility against microbial and insect attack in regulating pest populations and their impacts on trees and forests. We will also investigate the role of host defense mechanisms in altering interactions between microbes and insects that collectively impact host fitness. We will address these questions in a highly integrated manner, looking at aspects of host defense ranging from the transcriptome to the proteome, to the metabolome, and from the single tree to host populations. In our group we already have the technical knowledge base to address these highly complex questions (Barto et al. 2008; Blodgett et al. 2005; Blodgett et al.2007; Bonello and Blodgett 2003; Bonello et al. 2008; Bonello et al. 2006; Eyles et al. 2007a; Eyles et al. 2007b; Luchi et al. 2005; Ockels et al. 2007; Wallis et al. 2008; Wang et al. 2006).(The Ohio State University). We will investigate the interactions among Monterey pines, pitch canker, and bark beetles in California native Monterey pine forests. We are continuing our studies of vector potential for two engaver beetle species (Ips spp.) and a cone beetle (Conophthorus radiatae). Methods are described in Storer et al 2004, Erbilgin et al 2008, and Erbilgin et al 2009). (UC Berkeley). We will investigate the relationship of site, stand, disease and the occurrence of aspen bark beetles in Wyoming and Colorado ( Colorado State University). We will investigate the interactions among the host plants (coast live oaks, California black oaks, and tanoaks), the sudden oak death pathogen, and bark and ambrosia beetles in native forests of Coastal California. . Presently we are sampling phloem tissue from: 1) trees that have survived in our plots where high levels of mortality have occurred; and 2) trees that have survived inoculation with P. ramorum. Analyses of phenolic compounds shown to inhibit growth of P. ramorum in vitro have been initiated (Ockels et al 2007). (UC Berkeley). We will examine effects of varying levels of aspen density and root pathogen inoculum on transfer of root disease to regeneration in partially cut spruce-fir stands. Root pathogen inoculum will be manipulated by locating plots in areas of high and low inoculum, and by removing inoculum with a bulldozer. (Utah State University). We will examine the effects of stand management practices (fertilization and/or thinning) on the interaction among trees (Douglas-fir and lodgepole pine), bark beetles, and their associated mycangial fungi (University of Idaho). A native species of long-horned beetle, the red oak borer Enaphalodes rufulus (Haldeman) has recently emerged as a significant agent of oak mortality in the Ozark and Ouachita Mountains of Arkansas. We will investigate the role of host tree suitability and mechanisms of host defense against stem boring insects in hardwood forests. (University of Arkansas) Mortality generated through competition and intraguild predation is not well understood in relation to the initiation and termination of southern pine beetle area-wide infestations. We will initiate research on the role of competition, specifically targeting pine sawyers (Monochamus species) and pine engravers (Ips species) in the dynamics of southern pine beetle populations. (University of Arkansas) Objective 2: Characterize feedbacks among bark beetle-microbial interactions and forest ecosystem processes. We will characterize the role of resource availability in modulating tree defense. To do this, we will conduct studies in both controlled and field situations using the tools described in published work (Barto et al. 2008; Blodgett et al. 2005; Blodgett et al. 2007; Bonello and Blodgett 2003; Bonello et al. 2008; Bonello et al. 2006; Eyles et al. 2007a; Eyles et al. 2007b; Kleczewski et al. 2008; Luchi et al. 2005; Ockels et al. 2007; Wallis et al. 2008; Wang et al. 2006). (The Ohio State University). We will characterize the genetic and genomics structure of MPB fungal associates. We have a draft sequence of Ophiostoma clavigera that we have so far exploited to generate highly polymorphic microsatellite loci that we have genotyped on the contemporary epidemic populations. The results show that we have distinct routes of spread, that include a Rocky Mountain path that follows a South-North Axis, a Northern path, that includes the nothernmost populations that recently crossed into Alberta, and a strictly Alberta population. We are also finding some gene flow between O. clavigera and L. longiclavatum, but this needs to be confirmed with further DNA analyses. If these results are confirmed, they will reveal a much more complex and intricate relationship between those and possibly other fungal associates, than previously thought. (Hamelin, U British Columbia). We will develop models of disease progression in native coastal oak forests in California so that we can predict the rate of mortality and species composition of the next forest. Methods are described in Kelly et al 2008 and in McPherson et al 2005 and McPherson et al 2009 (in manuscript). (UC Berkeley). We will determine the most effective silvicultural practices to regenerate Monterey pines in senescing native forests of California in order to increase resistance to pitch canker in future pine generations. (UC Berkeley). We will examine the effect of fertilization on tree resistance (resin flow and monoterpene content) and nutritional parameters in Douglas-fir and lodgepole pine. (University of Idaho). We will characterize genes that control parasitic fitness in the Dutch elm disease pathogen Ophiostoma novo-ulmi. Components of fitness that we will investigate include pathogenicity, asexual and sexual reproduction, yeast-mycelium dimorphism, response to abiotic and biotic stresses, and temperature growth responses. Genetic and genomic studies will be conducted under laboratory conditions (Et-Touil et al., 1999; Tadesse et al., 2003; Bouvet et al., 2007, 2008; Plourde et al. 2008), whereas controlled inoculations will be carried out in growth chambers and greenhouses (Et-Touil et al., 2005). Based on existing evidence that O. novo-ulmi has acquired genes from the closely related species O. ulmi (Et-Touil et al. 1999), we will further explore the potential of interspecific hybridization in the evolution of O. novo-ulmi and other ophiostomatoid fungi associated with bark beetles. We anticipate that many of our expected findings on O. novo-ulmi can be extrapolated to genetically less tractable fungal pathogens of trees. (Laval University). Objective 3: Integrate and apply knowledge gained from obj. 1 and 2 to forest ecosystems as influenced by emerging issues such as invasive species, global climate change, changing land use patterns and fire regimes, and multiple and conflicting societal demands. Using existing models and results developed under efforts addressing objectives 1 and 2, we will develop spatially explicit models of focal diseases and insect outbreaks for predicting effects at stand levels. These models will also serve as platforms for hypothesizing effects of changing factors on forest ecosystems. (Utah State University).

    Measurement of Progress and Results

    Outputs

    • Increased knowledge upon which to base forest management decisions.
    • Improved data on which to predict outbreaks, based on a) weather, b) root insects and pathogens, and c) defoliators.

    Outcomes or Projected Impacts

    • Alternatives to manage forests and increase/maintain production of ecosystem services.
    • Improved tools for predicting insect and disease outbreaks.
    • Professionals trained to deal with insect and disease outbreaks at ecosystem scales.

    Milestones

    (2011): We will facilitate a meeting of entomologists and pathologists to foster development of international collaboration to address critical forest pest problems.

    (2013): We will also summarize knowledge obtained in this project and its previous incarnations into predictive models for management use. We expect to develop and test at least three such models in the next five years.

    Projected Participation

    View Appendix E: Participation

    Outreach Plan

    Our ability to incorporate and apply the knowledge gained from the proposed collaborative work will necessarily vary with individual management objectives within various agencies. Several outlets for dissemination of information are available to project members. The project members have an established record of publication of results in refereed journals and the proceedings from professional conferences. We will continue publishing in these outlets. In addition, many project members are active participants of and present their research results to professional societies such as the Entomological Society of America, the Society of American Foresters, the Western Forest Insect Work Conference and the Western International Forest Disease Work Conference. Our members are actively involved with various land management agencies including university experimental forests (i.e. the University of Idaho Experimental Forest, T.W. Daniel Experimental Forest (Utah State University) and tribal lands (i.e. with the Nez Perce) and cooperative projects with USDA Forest Service. Members also participate in various demonstration projects (e.g. SAF field days) that are often attended by practicing land managers. During our next 5 years, we will meet at least twice with other regional research projects with similar interests to share our research plans and results with other scientists.

    Organization/Governance

    The governance for the project closely follows the recommended guidelines. Officers will serve a two year term, with a new secretary elected at the annual meeting of the project and the current secretary serving as the chair during the second year. Administrative guidance will be provided by our Administrative Advisor and a CSREES Representative.

    Literature Cited

    Aukema, B.H., & K. F. Raffa. 2005. Selective manipulation of predators using pheromones: Responses to frontalin and ipsdienol pheromone components of bark beetles in the Great Lakes region.. Agr. & For. Entomol. 7: 193-200.

    Aukema, B.H., Clayton, M, K. & K. F. Raffa 2005. Modeling flight activity and population dynamics of the pine engraver, Ips pini, in the Great Lakes Region: Effects of weather and predators over short time scales. Pop. Ecol. 47: 61-69.

    Baker, F. A. and McManus, W.J. 2007. Evidence of fungi in spruce roots from which fungi could not be cultured. Proc., 12th IUFRO Root and Butt Rot Conference p 206-208.

    Barto, E.K., S. Enright, A. Eyles, C.M. Wallis, R. Chorbadjian, R. Hansen, D.A. Herms, P. Bonello, and D.F. Cipollini. 2008. Effects of soil fertility on systemic protein defense responses of Austrian pine to attack by a fungal pathogen and an insect defoliator. Journal of Chemical Ecology 34:1392-1400.

    Bentz, et al. 2006. Bark Beetle Outbreaks in Western North America: Causes and Consequences. University of Utah Press.

    Bishop, R. J., and Jacobi, W. R. 2003. Insects associated with black stain root disease centers in pinyon pine stands. Southwestern Entomologist 78: 55-61.

    Blodgett, J. T., A. Eyles, and P. Bonello. 2007. Organ-dependent induction of systemic resistance and systemic susceptibility in Pinus nigra inoculated with Sphaeropsis sapinea and Diplodia scrobiculata. Tree Physiology 27:511-517.

    Blodgett, J.T., D.A. Herms, and P. Bonello. 2005. Effects of fertilization on red pine defense chemistry and resistance to Sphaeropsis sapinea. Forest Ecology and Management 208:373-382.

    Bonello, P., and J. T. Blodgett. 2003. Pinus nigra-Sphaeropsis sapinea as a model pathosystem to investigate local and systemic effects of fungal infection of pines. Physiological and Molecular Plant Pathology 63 (5):249-261.

    Bonello, P., T.R. Gordon, and A.J. Storer. 2001. Systemic induced resistance in Monterey pine. Forest Pathology 31:99-106.

    Bonello, P., N. Luchi, P. Capretti, and M. Michelozzi. 2008. Host-mediated effects of Heterobasidion annosum s.s. infection on severity of Diplodia pinea tip blight in Italian stone pine (Pinus pinea L.). Tree Physiology 28:16531660.

    Bonello, P., T. R. Gordon, D. A. Herms, D. L. Wood, and N. Erbilgin. 2006. Nature and ecological implications of pathogen-induced systemic resistance in conifers: A novel hypothesis. Physiological and Molecular Plant Pathology 68: 95-104.

    Bouvet, G.F., V. Jacobi, and L. Bernier. 2007. Characterization of three DNA transposons in the Dutch elm disease fungi and evidence of repeat-induced point (RIP) mutations. Fungal Genet. Biol. 44: 430-443.

    Bouvet, G.F., V. Jacobi, K.V. Plourde, and L. Bernier. 2008. Stress-induced mobility of OPHIO1 and OPHIO2, DNA transposons of the Dutch elm disease fungi. Fungal Genet. Biol. 45: 565-578.

    Cardoza, Y. J., K. D. Klepzig & K. F. Raffa. 2006. Bacteria in oral secretions of an endophytic insect inhibit antagonistic fungi. Ecol. Entomol. 31: 636-645.

    Cardoza, Y. J., K. D. Klepzig, J. C. Moser & K. F. Raffa. Raffa. 2008. Multipartite symbioses among fungi, mites, nematodes and the spruce beetle, Dendroctonus rufipennis. Environ. Entomol. In Press.

    Dahlsten, D. L., Six, D. L., Rowney, D. L., Lawson, A. B., Erbilgin, N., & K. F. Raffa. 2003. Attraction of Ips pini (Coleoptera: Scolytidae) and its predators to natural attractants and synthetic semiochemicals: Implications for population monitoring in northern California. Environ. Entomol. 32: 1115-1122.

    Dahlsten, D. L., Six, D. L,. Erbilgin, N., Raffa K. F., Lawson, A. B., & D. L. Rowney. 2004. Attraction of Ips pini (Coleoptera: Scolytidae) and its predators to various enantiomeric ratios of ipsdienol and lanierone in California: Implications for the augmentation and conservation of natural enemies. Environ. Entomol. 33: 1554-1561.

    Delalibera I., Jr., Vasanthakumar, A., Burwitz, BJ, Schloss, PD, Klepzig, KD, Handelsman J & K.F. Raffa, 2007. Composition of the bacterial community in the gut of the pine engraver beetle, Ips pini (Say) (Coleoptera: Curculionidae: Scolytinae). Symbiosis. 47: 93-104.

    Erbilgin, N., S. Mori, J.H. Sun, J.D. Stein, D.R. Owen, L.D. Merrill, R. Campos Bolanos, K.F. Raffa, J. Mendez Montiel, D.L. Wood, and N.E, Gillette. 2007. Response to host volatiles by native and introduced populations of Dendroctonus valens (Coleoptera: Curculionidae, Scolytinae) in North America and China. J. Chem. Ecol. 33(1): 131-146.

    Erbilgin, N., Ritokova, G., Gordon, T.R., Wood, D.L., and Storer, A.J. 2008a. Temporal variation in contamination of pine engraver beetles with Fusarium circinatum in native Monterey pine forests in California. Plant Pathology Doi: 10.1111/j.1365-3059.2008.01887.x.

    Erbilgin, N. 2009. Bark beetle (Coleoptera: Scolytidae)-mediated fungal infections of susceptible trees induce resistance to subsequent infections in a dose dependent manner. Agricultural and Forest Entomology (in press).

    Et-Touil, A., C.M. Brasier, and L. Bernier. 1999. Localization of a pathogenicity gene in Ophiostoma novo-ulmi and evidence that it may be introgressed from O. ulmi. Mol. Plant Microbe Interact. 12: 6-15.

    Et-Touil, A., D. Rioux, F. Mathieu, and L. Bernier. 2005. External symptoms and histopathological changes following inoculation of genetically close strains of Ophiostoma to elms putatively resistant to Dutch elm disease. Can. J. Bot. 83: 656-667.

    Eyles, A., R. Chorbadjian, C.M. Wallis, R.C. Hansen, D.F. Cipollini, D.A. Herms, and P. Bonello. 2007. Cross-induction of systemic induced resistance between an insect and a fungal pathogen in Austrian pine over a fertility gradient. Oecologia 153: 365-374.

    Eyles, A., K. Riedl, W. Jones, S. Schwartz, K. Chan, D.A. Herms, D.F. Cipollini, and P. Bonello. 2007. Comparative phloem chemistry of Manchurian (Fraxinus mandshurica) and two North American ash species (F. americana and F. pennsylvanica). Journal of Chemical Ecology 33:14301448.

    Garriston-Johnston, M.T., J.A. Moore, S.P. Cook, & G.J. Niehoff. 2003. Douglas-fir beetle infestations are associated with certain rock and stand types in the Inland Northwestern United States. Environ. Entomol. 32: 1354-1363.

    Gordon, T.R., Storer, A.J., and Wood, D.L. 2001. The Pitch Canker Epidemic in California. Plant Disease 85: 1128-1139.

    Jacobi, W. R., Koski, R. D., Harrington, T.C. and Witcosky, J. J. 2007. Association of Ophiostoma novo-ulmi with Scolytus schevyrewi Semenov (Scolytidae) in Colorado. Plant Disease: 91: 245-247.

    Jacobi, W.R., Zeglan, S. and Beale, J.D. 2008. Black stain root disease progression in coastal Douglas-fir in British Columbia. Can. J. Plant Pathol. 30: 339-344.

    Kallas, M. A., Reich, R. M., Jacobi, W. R., and Lundquist, J. E. 2003. Modeling the probability of observing Armillaria root disease in the Black Hills. Forest Pathology 33:241-252.

    Kearns, H.S. J. and Jacobi, W.R. 2005. Impacts of black stain root disease in recently formed mortality centers in the piñon  juniper woodlands of Southwestern Colorado. Can. J. For. Res. 35: 461-471.

    Kearns, H.S.J and Jacobi. W.R. 2007. The distribution and incidence of white pine blister rust in central and southeastern Wyoming and northern Colorado. Can. J. For. Res.: 37:1-11.

    Kelly, M., Liu, D., McPherson, B., Wood, D., and Standiford, R. 2008. Spatial pattern dynamics of oak mortality and associated disease symptoms in a California hardwood forest affected by sudden oak death. Journal of Forest Research 13: 312-319.

    Kleczewski, N.M., D.A. Herms, and P. Bonello. 2008. Fertility effects on ectomycorrhizal abundance and primary and secondary metabolism of paper birch (Betula papyrifera): Integrating models of optimal allocation, mycorrhizal regulation, and the growth-differentiation balance hypothesis. New Phytologist In review.

    Klepzig, K.D., K.F. Raffa, & E.B. Smalley. 1991. Association of insect-fungal complexes with Red Pine Decline in Wisconsin. For. Sci. 37: 1119-1139.

    Klutsch, J.G., R.D. Beam, W.R. Jacobi, J.F. Negron. 2007. Fuel and stand characteristics in ponderosa pine infested with mountain pine beetle, Ips beetle, and southwestern dwarf mistletoe in Colorados northern Front Range. In: Proceedings of the 55th Annual Western International Forest Disease Work Conference; 10/15/2007, Sedona, AZ. [Abstract].

    Lee, J.C., Haack, R.A., Negron, J.F., Witcosky, J.J., and Seybold, S.J. 2007. Invasive Bark Beetles. Forest Insect and Disease Leaflet 176, United State Department of Agriculture, U.S. Forest Service.

    Logan, J.A., Regniere, J, and Powell, J.A., 2003. Assessing the impacts of global warming on forest pest dynamics. Front. Ecol. Environ 1:130-137.

    Luchi, N., R. Ma, P. Capretti, and P. Bonello. 2005. Systemic induction of traumatic resin ducts and resin flow in Austrian pine by wounding and inoculation with Sphaeropsis sapinea and Diplodia scrobiculata. Planta 221 (1):75-84.

    McNee, W.R., Bonelo, P., Storer, A.J., Wood, D.L., and Gordon, T.R. 2003. Feeding response of Ips paraconfusus to phloem and phloem metabolites of Heterobasidion annosum-inoculated ponderosa pine, Pinus ponderosa. Journal of Chemical Ecology 29 (5): 1183-1202.

    McPherson BA, Mori SR, Wood DL, Storer AJ, Svihra P, Kelly NM, Standiford RB. 2005. Sudden oak death in California: Disease progression in oaks and tanoaks. Forest Ecology & Management 213: 71-89.

    McPherson, B.A., Erbilgin, N., Wood, D.L. Svihra, P., Storer, A.J. and Standiford, R.B. 2008. Attraction of ambrosia and bark beetles (Coleoptera: Scolytidae) to coast live oaks (Quercus agrifolia) infected by Phytophthora ramorum. Agricultural and Forest Entomology 10: 315-321.

    Ockels, F.S., A. Eyles, B.A. McPherson, D.L. Wood, and P. Bonello. 2007. Chemistry of coast live oak response to Phytophthora ramorum infection. Journal of Chemical Ecology 33 (9):1721-1732.

    Omdal, D. W. Shaw, C. G. III, and Jacobi, W. R. 2004. Symptom expression in conifers infected with Armillaria ostoyae and Heterobasidion annosum. Can. J. For. Res. 34: 1210-1219

    Owen, D.R., Wood, D.L., and Parmeter, J.R. 2005. Association between Denroctonus valens and black stain root disease on ponderosa pine in the Sierra Nevada of California. Canadian Entomologist 137: 367-375.

    Plourde, K.V., V. Jacobi, and L. Bernier. 2008. Use of insertional mutagenesis to tag putative parasitic fitness genes in the Dutch elm disease fungus Ophiostoma novo-ulmi subsp. novo-ulmi. Can. J. Microbiol. 54: 797-802.

    Raffa, K.F., Hobson, K.R., LaFontaine, S., & B. H. Aukema. 2007. Can chemical communication be cryptic? Adaptations by herbivores to natural enemies exploiting prey semiochemistry. Oecologia. 153: 1009-1019.

    Raffa, K.F. & E.B. Smalley. 1995. Interaction of pre-attack and induced monoterpene concentrations in conifer defense against bark beetle-microbial complexes. Oecologia. 102: 285-295.

    Rebek, E.J., D.A. Herms, and D.R. Smitley. 2008. Interspecific variation in resistance to emerald ash borer (Coleoptera: Buprestidae) among North American and Asian ash (Fraxinus spp.). Environmental Entomology 37 (1):242-246.

    Regniere, J.and Bentz, B.J. 2007. Modeling cold tolerance in the mountain pine beetle Dendrotoctonus ponderosae. J. Insect Physiol. 53:559-572.

    Seybold, S.J. and Tittiger, C. 2003. Biochemistry and Molecular Biology of de novo Isoprenoid Pheromone Production in the Scolytidae. Annual review of Entomology 48: 425-453.

    Storer, A.J., Wood, D.L., and Gordon, T.R. 2004. Twig beetles, Pityophthorus spp. (Coleoptera: Scolytidae) as vectors of the pitch canker pathogen in California. Canadian Entomologist 136: 685-693.

    Tadesse, Y., L. Bernier, W.E. Hintz, and P.A. Horgen. 2003. Real time RT-PCR quantification and Northern analysis of Cerato ulmin (CU) gene transcription in different strains of the phytopathogens Ophiostoma ulmi and O. novo ulmi. Mol. Genet. Genomics 269 :789-796.

    Tillman, J.A., Seybold, S.J., Jurenka, R.A., and Blomquist, G.J. 1999. Insect pheromones  an overview of biosynthesis and endocrine regulation. Insect Biochemistry and Molecular Biology 29: 481-514.

    Wager, D.J., Baker, F.A. 2006. Ozone concentrations in Utah's Central Wasatch Mountains. J. Air and Waste Mgmt. 56:1381-1390.

    Wallin, K.F., & K.F. Raffa. 2004. Feedback between individual host selection behavior and population dynamics in an eruptive insect herbivore. Ecol. Monogr. 74: 101-116.

    Wallis, C.M., A. Eyles, R. Chorbadjian, B.B. McSpadden-Gardner, R. Hansen, D.F. Cipollini, D.A. Herms, and P. Bonello. 2008. Systemic induction of phloem secondary metabolism and its relationship to resistance to a canker pathogen in Austrian pine. New Phytologist 177:767778.

    Wang, D., A. Eyles, D. Mandich, and P. Bonello. 2006. Systemic aspects of host-pathogen interactions in Austrian pine (Pinus nigra): a proteomics approach. Physiological and Molecular Plant Pathology 68:149-157.

    Wood, D.L. 1982. The role of pheromones, kairomones, and allomones in the host selection and colonization behavior of bark beetles. Annual Review of Entomology 27: 411-446.

    Attachments

    Land Grant Participating States/Institutions

    AR, CA, CO, ID, KY, MN, MS, MT, OH, OR, UT, WI

    Non Land Grant Participating States/Institutions

    Laval University
    • Log Out ?

    Are you sure you want to log out?

    Press No if you want to continue work. Press Yes to logout current user.

    Yes
    Report a Bug
    Report a Bug

    Describe your bug clearly, including the steps you used to create it.