Mechanisms and Deployment of Resistance in Trees to Insects

Mechanisms and Deployment of Resistance in Trees to Insects

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Mechanisms and Deployment of Resistance in Trees to Insects Edited by

Michael R. Wagner School of Forestry, Northern Arizona University, Flagstaff, AZ, U.S.A.

Karen M. Clancy Rocky Mountain Research Station, Flagstaff, AZ, U.S.A.

François Lieutier Université d’Orléans, Orléans, France and Institut National de la Recherche Agronomique, Orléans, France

and

Timothy D. Paine Department of Entomology, University of California, Riverside, CA, U.S.A.

KLUWER ACADEMIC PUBLISHERS NEW YORK, BOSTON, DORDRECHT, LONDON, MOSCOW

eBook ISBN: Print ISBN:

0-306-47596-0 1-4020-0618-7

©2002 Kluwer Academic Publishers New York, Boston, Dordrecht, London, Moscow Print ©2002 Kluwer Academic Publishers New York All rights reserved No part of this eBook may be reproduced or transmitted in any form or by any means, electronic, mechanical, recording, or otherwise, without written consent from the Publisher Created in the United States of America Visit Kluwer Online at: and Kluwer's eBookstore at:

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Table of Contents Preface Acknowledgement

vii ix

Chapter 1 Resistance in trees to insects – An overview of mechanisms and 1 interactions .... S. LARSON Chapter 2 Mechanisms of resistance in conifers and bark beetle attack strategies F. LIEUTIER Chapter 3 Mechanisms of resistance in trees to defoliators K. CLANCY

31 79

Chapter 4 Mechanisms of resistance in conifers against shoot infesting insects.The case of the white pine weevil Pissodes strobi (Peck) (Coleoptera: Curculionidae) 105 R. I. ALFARO, J. H. BORDEN, J. N. KING, E. S. TOMLIN, R. L. MCINTOSH, J. BOHLMANN Chapter 5 Host tree resistance to wood-boring insects T. D. PAINE Chapter 6 Plant resistance against gall-forming insects: the role of hypersensitivity ....... T. G. CORNELISSEN, D. NEGREIROS, G.W. FERNANDES

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Chapter 7 The resistance of hybrid willows to specialist and generalist herbivores and pathogens: the potential role of secondary chemistry and parent host plant status 153 J. HJÄLTÉN, P. HALLGREN Chapter 8 Deploying pest resistance in genetically-limited forest plantations: developing ecologically-based strategues for managing risk

D. J. ROBISON

169

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Chapter 9 Deployment of tree resistance to insects in short-rotation Populus plantations D. R. COYLE, J. D. MCMILLIN, R. B. HALL, E. HART

189

Chapter 10 Strategies for Deployment of Insect Resistant Ornamental Plants D. A. HERMS

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Chapter 11 Possibilities to utilize tree resistance to insects in forest pest management in central and western Europe 239 C.M. HEIDGER and F. LIEUTIER Chapter 12 Deployment of tree resistance to pests in Asia N. KAMATA.

265

Chapter 13 Using resistance in tropical forest plantations ... J. D. NICHOLS, M. R. WAGNER, J. R. COBBINAH

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Keyword Index Species Index

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Preface

This book is the result of an international symposium that was held in Iguassu Falls, Brazil August 20-26, 2000 as part of the International Congress of Entomology. The symposium was organized by the International Union of Forest Research Organizations (IUFRO) Working Party S7.01.02, Tree Resistance to Insects which is part of the IUFRO Subject Group S7.01 – Physiology and Genetics of Tree-Phytophage Interactions. The organizers of this symposium were the editors of this book and all are members of the IUFRO Working Party. Contributors were invited members of the IUFRO Working Party with particular knowledge in some aspect of deployment and mechanisms of resistance. All papers presented in this book were peer reviewed prior to their acceptance. This book reviews the major worldwide literature on mechanisms and deployment of resistance in trees to insects. General patterns in the mechanisms of resistance for defoliators, shoot insects, wood borers, bark beetles, and gall forming insects are presented. Strategies for deployment of tree resistance in short-rotation biomass plantations, horticulture, and natural forests are discussed. Regional patterns of deployment of resistance for Europe, Asia, and Tropical Forests illustrate the extent to which foresters are currently using environmentally appropriate genetic resistance as a pest management tool. Overview chapters synthesize many of the broad patterns and provide guidance for future research and implementation of genetic resistance in trees to insects.

Michael R. Wagner Karen M. Clancy Francois Lieutier Timothy D. Paine

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Acknowledgment

The authors gratefully acknowledge the generous support of Northern Arizona University School of Forestry McIntire-Stennis Program; the USDA Forest Service Research and Development, Rocky Mountain Research Station and the University of California-Riverside University of California-Riverside Department of Entomology for partial underwriting of the cost of printing and distribution of this book. Special thanks to Yiqun Lin, Northern Arizona University School of Forestry for editorial assistance and to Maia Dickerson at the Rocky Mountain Research Station for assistance in checking the literature citations. Finally our thanks to all members of the IUFRO Working Party S7.01.02 Tree Resistance to Insects for the many years of free exchange of ideas about tree resistance to insects that make this type of overview publication possible.

Michael R. Wagner Karen M. Clancy Francois Lieutier Timothy D. Paine

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CHAPTER 1 RESISTANCE IN TREES TO INSECTS – AN OVERVIEW OF MECHANISMS AND INTERACTIONS

STIG LARSSON

Department of Entomology, Swedish University of Agricultural Sciences, Box 7044,SE-750 07 Uppsala, Sweden

1. INTRODUCTION The use of insect-resistant plant varieties is an important part of integrated pest management in agriculture. Classic breeding for insect resistance includes extensive screening of a large number of genotypes in a common environment, selection of the most promising genotypes for testing in field trials, and then production of new crosses based on data from field tests (Maxwell and Jennings 1980). Forest management has, on the other hand, to handle long rotation times, in certain ecosystems a hundred years or more. Obviously, under such circumstances it is not easy to apply the traditional breeding techniques developed for agricultural crops. Consequently, few tree genotypes exist that have been intentionally bred for resistance against insects (Hanover 1980). There is no doubt, however, that tree resistance plays an important role in the ecology of forest insects. Variation in traits likely to confer resistance to insects has been found within many natural plant populations, including trees (Marquis 1992). In managed forests, damage caused by insects varies among stands, varieties (provenances, clones), and individual trees, sometimes due to documented differences in resistance (Leather 1996). An often discussed aspect of tree resistance is the suggested abiotic induction of tree susceptibility that may trigger insect outbreaks (Mattson and Haack 1987). Although it has long been accepted that tree resistance needs to be considered in insect pest management models (Stark 1965), it has been difficult to achieve this goal because of the poor mechanistic understanding of the resistance. However, the 1 M.R. Wagner et al. (eds.), Mechanisms and Deployment of Resistance in Trees to Insects, 1–29. © 2002 Kluwer Academic Publishers. Printed in the Netherlands.

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last two decades have seen an impressive development of conceptual models on mechanisms involved in the interaction between plant and insect. Initially, plant/insect interactions were studied mainly from an ecological perspective. In recent years, breakthroughs in molecular techniques have made it possible to address questions at the cellular level. A challenge for the future will be to combine the ecological and the molecular paradigms in order to develop reliable models of tree resistance. Such models will be important for ecologists who aim to explain the abundance and distribution of insect populations, as well as for forest managers who aim to include resistant tree genotypes into forest pest management strategies. In order for such models to be successful, we need to acknowledge that questions asked at different levels of organization, i.e., cell, individual, population, will inevitably yield different kinds of answers. It will be essential to develop research tools that view resistance mechanisms from this variety of organization levels (Rausher 2001). 2. CONCEPTS AND DEFINITIONS The resistance concept has its roots in plant breeding research (e.g., Painter 1958; Maxwell and Jennings 1980). During recent years ecologists have elaborated on the breeding concepts but without consistency in terminology. This is not the place to thoroughly discuss the conceptual basis of resistance and related terms, but it is important to define a few key concepts. For the purpose of this chapter I follow, with some modifications, the definitions proposed by Karban and Baldwin (1997), and Strauss and Agrawal (1999). This view is different from the Painter (1958) definition in that it separates resistance from tolerance (see Fig. 1). Painter’s definition focuses on damage to the plant; any plant characters that minimize damage will contribute to resistance, be they toxins, deterrents or compensatory processes. Thus, he viewed compensation, or tolerance, as one component of resistance, and others after him have adopted this view (e.g., Berenbaum and Zangerl 1992a). Research during the last decade has emphasized the importance of tolerance as a plant strategy to reduce negative effects of herbivory (Stowe et al. 2000; Haukioja and Koricheva 2001). It appears that resistance and tolerance may be alternatives, and because they both carry costs they cannot simultaneously be maximized in one and the same plant genotype (Fineblum and Rausher 1995). Thus, there are good theoretical reasons to treat them as qualitatively different solutions for reducing fitness costs in response to herbivory. Still, our understanding of tolerance lags behind that of resistance, although tolerance may be much more important than generally acknowledged (Hjältén et al. 1993). Resistance as defined here is not primarily related to plant damage, as opposed to Painter's (1958) definition, but instead focuses on the negative effect a resistant plant has on the target herbivore. It is important to separate the concept of resistance into its two parts, the plant component, the resistant trait, and the insect response (behavioral or physiological) to this trait. I consider the interaction between the plant trait and the insect response to constitute the mechanism of resistance (see Fig. 1). Thus defined, a resistance mechanism cannot be described unless both the plant trait

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and the target herbivore are identified. A resistance trait such as a toxic chemical, trichomes, or thick bark can have evolved in response to a number of selection pressures, including UV-radiation, frost, drought, microorganisms, mammals, plant competition, as well as to herbivorous insects (Marquis 1992). Such a trait may, or may not, negatively influence the insect herbivore under study. Nevertheless, it is convenient to classify the character as a resistance trait as long as we know that it negatively affects some insect(s), or on logical grounds can be supposed to do so. In order to talk about a mechanism of resistance, however, we have to require that the insect responds negatively when exposed to the resistance trait (Fig. 1).

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The negative effect on the insect can be of two kinds. It can either result in an avoidance behavior, oviposition or feeding, whereby the insect is deterred by the plant trait (antixenosis). Alternatively, the resistance trait can interfere with the physiology of the insect, once it has accepted to feed on the plant, leading to reduced growth, fecundity, or survival (antibiosis). "Non-host resistance" is a term used in plant pathology to describe the inability of a pathogen to infect a plant “due to lack of something in the plant that the pathogen needs or to the presence of substances incompatible with the pathogen” (Agrios 1997; also cf. Heath 2000). It is interesting to note that this term is seldom used in the insect literature although the avoidance behavior shown by an insect to a plant that is not part of its host range is highly analogous to non-host resistance against microorganisms. One important difference between microorganisms and insects is that the latter have behaviors. Because insect behaviors related to feeding and oviposition often are context dependent, it may be difficult to describe what is non-host resistance to a particular insect species. A rich literature exists on the plasticity of insect behavior when it comes to host acceptance. For example, age, egg load, plant abundance, and previous experience are factors known to modify acceptance of a plant for feeding and oviposition (Finch and Collier 2000; Papaj 2000; Hopkins and van Loon 2001). It should be emphasized that the definitions used here do not necessarily imply that a resistant plant will be damaged less than a more susceptible plant (although that would most often be the case). For example, sub-lethal effects of a particular resistance trait on insect growth can lead to compensatory feeding whereby more plant tissue is consumed on a resistant plant than on a less resistant one (e.g., Winterer and Bergelson 2001). The concept of defense has been suggested to account for plant characters that in fact protect the plant (Karban & Baldwin 1997). This view is followed here, but others have different perspectives on the concept of defense. In particular, it has been proposed that the term defense implies something about evolutionary history, i.e. that the trait in question has evolved because of selection from herbivores (Rausher 1992). Traditionally, resistance has been considered as genetically determined, probably because of the strong influence from plant breeders in agriculture (e.g., Painter 1958). Ecologists have increasingly used resistance more broadly. Especially when it comes to tree/insect interactions the term resistance is frequently referred to as a phenotypic feature possibly shaped by biotic as well as abiotic factors (e.g., Christiansen et al. 1987; Hanks et al. 1991; Wagner and Zhang 1993).

3. RESISTANCE TRAITS Plant characteristics known to influence insect preference and performance include (1) primary metabolites, (2) secondary metabolites, (3) physical factors, and (4) phenology. Current research increasingly emphasizes interactions among these

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features (Schopf 1986; Duffey and Stout, 1996; Tomlin and Borden 1997; Kause et al., 1999a; Nelson and Kursar 1999). 3.1 PRIMARY METABOLITES Nitrogen is by far the most important nutrient for insect growth and survival (Mattson 1980, Mattson and Scriber 1987). Many insects have evolved life history traits to maximize nitrogen uptake from plant tissue low in nitrogen, in comparison to their needs (Slansky 1993). It is worth pointing out that plant-feeding insects most likely are sensitive to the composition of nitrogenous compounds, and thus total nitrogen can be misleading when judging the suitability of a particular plant (Felton 1996; Sandström and Moran 1999). Carbohydrates have largely been ignored in plant/insect studies probably based on the assumption that energy does not limit growth of herbivorous insects. A number of recent studies indicate, however, that single carbohydrate compounds are essential ingredients in the food of arboreal caterpillars (Jensen 1988; Clancy et al. 1993; Suomela et al. 1995). There is much variation in concentrations of primary metabolites within species growing in different habitats, within species of different age, as well as among tissue types within plant individuals (Clancy et al. 1995). Because there is so much variation that is seemingly of ontogenetic and physiological origin primary metabolites are rarely considered to be part of plant resistance, although this may be erroneous (Berenbaum 1995). 3.2. SECONDARY METABOLITES A multitude of studies have documented genetic variation in secondary metabolites, such as terpenoids, phenolics, and alkaloids and the negative effects that these compounds have on insect performance (Rosenthal and Berenbaum 1992). In contrast to primary metabolites, there is a tremendous interspecific variation in the composition and concentration of secondary metabolites (Harborne 1993). In addition, there is also a considerable variation among genotypes within a species (e.g., Orians et al 1996; Osier et al. 2000), among plant individuals of different age (Fritz et al. 2001), among branches within the canopy (Carisey and Bauce 1997), and among leaf ages within individual branches (Ikeda et al. 1977; Wait et al. 1998). Many secondary metabolites are highly toxic to insects. In order to exploit plant tissue containing secondary metabolites insects have evolved behavioral adaptations to avoid the chemicals (Dussourd 1993), or efficient detoxification systems (Brattsten 1992). Presumably, biochemical adaptations are costly (Berenbaum and Zangerl 1992b) and have been considered to be the prime reason for the widespread specificity in plant use among herbivorous insects. For example, 16 out of 72 needle-eating insect species on Scots pine Pinus sylvestris in Sweden feed only on the genus Pinus (Björkman and Larsson 1991). However, other phenomena, e.g., escape from natural enemies, also are likely to contribute to the high degree of host plant specialization in herbivorous insects (Bernays and Graham 1988; Stamp 2001).

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Secondary metabolites can be constitutive, i.e. always present in the plant, or induced by insect feeding (Karban and Baldwin 1997). Constitutive compounds are often used as cues by insects when selecting host plant for feeding or oviposition (Byers 1995, Roininen et al. 1999). Thus, for adapted insects, i.e. those that have evolved the biochemical machinery that allows them to feed on otherwise toxic plants, secondary metabolites generally do not act as resistance traits. On the contrary, the secondary metabolites are essential for guiding the insect to the right plant. It should be remembered, however, that constitutive secondary metabolites protect the plant from the majority of non-adapted insects, obviously by means of deterring them from encounters (Bernays and Chapman 1976). Even specialist insects can be influenced negatively by high concentrations of secondary compounds in their natural food plant (Larsson et al. 1986; Zangerl and Berenbaum 1993). Increased concentrations of secondary metabolites observed as a result of induction by an attacking insect have received much attention in recent years. Many types of chemicals are found in higher concentrations following induction, including phenolic compounds in mountain birch induced by the autumnal moth (Kaitaniemi et al. 1998), tannins in oak after feeding damage by the gypsy moth (Rossiter et al. 1988), and terpenoids and phenolics after attack by bark beetles (Raffa 1991). A great number of hypotheses have been developed to explain the distribution of secondary metabolites among plant species and within plant individuals. In general, two types of hypotheses prevail. On one hand are models that take an evolutionary approach and aim to understand patterns of secondary metabolites among plant species with different life histories and growing in different habitats, emphasizing aspects such as optimality (McKey 1979), plant apparency (Feeny 1976), and resource availability (Coley et al. 1985). Another set of models focuses on variation in ecological time with predominantly ecophysiological explanations, pointing at hierarchies in allocation of resources (Waring and Pitman 1985), the balance between carbon and nutrient availability (Bryant et al. 1983), balance between growth and differentiation (Loomis 1932, Lorio 1986), and sink/source regulation (Honkanen and Haukioja 1998). Recently, attempts have been made to integrate the evolutionary and ecological/physiological perspective (Herms and Mattson 1992; Koricheva et al. 1998a; Jones and Hartley 1999). When testing these hypotheses, and when suggesting improvements (Hamilton et al. 2001), it is important to take into account the different time scales on which they operate (Coley and Barone 1996) and whether the focus is on constitutive or induced resistance (Lombardero et al. 2000). It is also important to keep in mind that although all the models were initially developed within a plant/herbivore framework, most of them make predictions about plant traits, in particular traits assumed to have a defensive function. Thus, most models cannot be tested by simply performing bioassays with randomly chosen species of insects, a common practice in the past, because of general problems related to seemingly idiosyncratic insect responses (e.g., Lindroth et al. 1993; Hemming and Lindroth 1995; Ikonen et al. 2001).

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3.3. PHYSICAL FACTORS The toughness of plant structures is a serious hurdle for many herbivorous insects. Toughness of leaves on woody plants varies among taxa (Coley 1983), within taxa among habitats (Shure and Wilson 1993), and among age classes within a species (Larsson and Ohmart 1988). Most likely, tough leaves hinder many non-adapted insects from initiating feeding, although this source of resistance is difficult to separate from chemical traits. Even adapted insects find it difficult to feed on the tough leaves of certain plants. For example, neonate larvae of the leaf beetle Paropsis atomaria can only establish feeding on the very tender young leaves of its host Eucalyptus blakelyi; larvae will suffer very high mortality if these leaves for some reason are not available, e.g., because of extended drought or defoliation by another herbivore (Larsson and Ohmart 1988). In many plants the surface of buds, leaves and young shoots is covered by hairs that can be morphologically and functionally very diverse (Werker 2000). It is generally assumed that hairs can act as a resistance trait against insects (Levin 1973). For example, experimental removal of the hairs from young willow leaves make them more accessible for leaf beetle larvae (Rowell-Rahier and Pasteels 1982). Leaves on certain plant species have trichomes with glands containing secondary metabolites (Duffey 1986), thus a combination of a chemical and a physical trait. Such glandular trichomes affect insect feeding and movement through the action of the glandular exudate that may trap or deter the insect. Many examples of plants with glandular trichomes providing resistance against insects exist in the agricultural literature. Hairs are present on many woody plants, especially in young tissue (e.g., Denno et al. 1990), but their ecological importance has not been extensively investigated (Zvereva et al. 1998). 3.4. PHENOLOGY Many insects are specialized not only to a particular plant taxon but also to a particular tissue type. This represents a considerable risk for the insect if the tissue is available for only a short period in time, which is the case, for example, with the budbreak of perennial plants in temperate regions. There is variation in timing of budbreak at several spatial levels, i.e., among plant populations (Lawrence et al. 1997), among individuals within a population (Hunter 1992, Quiring 1994), among branches within plant individuals (Carroll and Quiring 1994) and among buds within a branch (Quiring 1993). Such variation may have consequences for the growth and survival of associated herbivores, and the strength of the effect depends on insect life history traits, e.g., degree of tissue specialization, dispersal capacity, and life span. In particular, insects with short life spans and an extreme dependence on a particular growth phase are vulnerable to such variation, e.g., galling cecidomyiids that depend on undifferentiated tissue for successful gall initiation (Yukawa 2000). In natural systems insect life history is synchronized with seasonal development of the preferred plant tissue. This means that most insect individuals in most years successfully can exploit the food resource. However, the resources - plant

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individuals, branches, or buds - that for some reason are out of synchrony with the main part of the resource population will be resistant. Exploiting asynchrony between tree and insect pest could possibly be an important part of integrated pest control (Hulme 1995). However, recent studies on effects on the population ecology of lepidopterans have found little support for asynchrony playing an important role (Hunter 1993; Watt and Woiwod 1999; but see Thomson et al. 1984). Insects with a more intimate association with the host plant, such as galling insects, may be more vulnerable to asynchrony (Isaev et al. 1988). Plant phenology, in the sense of, for example, seasonal development of leaf morphology or shoot length, is almost always accompanied by changes in chemistry. Development and chemistry in growing oak leaves is a classic example; protein concentrations decrease and tannin concentrations increase as leaves mature and get tougher (Feeny 1970). Recent work by Salminen et al. (2001) demonstrates intricate within-season dynamics in the composition and concentrations of tannins in birch leaves, with consequenses for insect growth (Ossipov et al. 2001). Thus, in cases where chemistry has been thoroughly investigated great changes in concentrations with aging of the plant tissues have always been detected. Therefore, what is generally labeled a "phenological" trait is probably most often of a chemical or physical nature. The extremely dynamic conditions in growing tissue can also be a serious methodological problem. Koricheva (1999) pointed out that many ecological studies of secondary metabolites do not make appropriate distinctions between concentration and content, a problem that is especially frequent when studying rapidly growing tissue. 3.5. THE IMPORTANCE OF TRADE-OFFS IN DETERMINING LEVEL OF RESISTANCE It is central to theories about plant resistance that there is a cost associated with the construction and maintenance of traits conferring resistance (McKey 1979; Simms 1992). If there is a cost, then there is the potential for trade-offs, meaning “a negative association between two traits seen in the phenotypic expression” (Mole 1994). One trade-off that has been widely discussed is that between growth and defense (Fagerström et al. 1987; Herms and Mattson 1992). Surprisingly often the expected negative relationships between these two functions have been difficult to document (Simms and Rausher 1989; Rousi et al. 1993; but cf. Bergelson and Purrington 1996). Recently, Koricheva (2002) concluded from a meta-analysis that the magnitude of the trade-off varies depending on whether it is measured at the level of phenotype or genotype; the average magnitude of among-genotype correlations was higher than that of among-phenotype correlations. It is also important to remember that there are different kinds of costs. Most often trade-offs refer to allocation costs, i.e., cost of production, transport, storage, and maintenance. Two other costs may also be important to consider. Opportunity costs occur when the plant loses in competition because it invests in resistance early in ontogeny (Coley et al. 1985). Ecological costs can come about if a trait that confers resistance to one insect species results in increased susceptibility to another, or negatively

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influences natural enemies (van Dam and Hare 1998) or pollinators (Strauss et al. 1999). A much less studied but potentially important trade-off is the one between different kinds of resistance traits. Again, if there is a cost, then one would expect trade-offs between different resistance traits. For example, leaf toughness and trichome density is negatively correlated in Rubus bogotensis (Björkman and Andersson 1990). The fact that different resistant traits respond differently to environmental factors (e.g., Björkman et al. 1998) can also be the result of trade-offs and competition for common resources (Haukioja et al. 1998). Obviously, we need to know more about trade-offs between growth and resistance, and among different resistant traits, if we are to understand the evolution of resistance and to develop insect-resistant plant genotypes. It is generally accepted that resistance has had to be compromised with other desirable traits in highyielding agricultural crops (Rosenthal and Dirzo 1997). Fewer efforts have been made concerning resistance breeding in forestry (Hanover 1966), and thus we know less about the importance of trade-offs in woody plants. But because the underlying resource base for trade-offs is larger, it is possible that the magnitude of the effect is smaller in trees than in cereal crops (cf. Mole 1994). 4. INSECT RESPONSES As defined here, resistance mechanisms constitute the action of a plant trait on the insect under study. I consider this perspective to be essential because whether or not a particular plant characteristic is manifested as a resistance trait depends on the response of the insect. Many insects adapted to feed on a plant species with, for example, high concentrations of secondary metabolites will suffer small or no negative effects on individual performance (e.g., Larsson et al. 1992); by definition (Karban & Baldwin 1997), such a plant has low or no resistance to that insect. What we call adapted insects have evolved life history traits that allow them to cope with resistance traits such as low tissue nitrogen concentration, high concentrations of secondary metabolites, adverse physical features such as tough leaves, or short temporal windows in suitability. It is generally believed that specialized insects are better equipped to handle potent resistance traits, although there does not seem to be a straightforward correlation (Jaenike 1990). Most natural plant populations exhibit polymorphism with respect to resistance traits so that resistance is overexpressed in certain plant individuals (e.g., Osier et al. 2000). On such plants even highly specialized insects can suffer reduction in growth and survival (Fig. 2).

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Much progress has been made in recent years with respect to understanding the responses of insect individuals to variable plant resistance traits (e.g., Brewer et al. 1985; Ayres et al. 1997; Hwang & Lindroth 1997, Ossipov et al. 2001). Unfortunately, for most plant/insect interactions we still only have qualitative information, i.e., statistically significant effects have been documented for one or at the most a few doses of the resistance trait. Although such information is essential in order to develop hypotheses covering qualitative relationships, it is of limited value when extrapolating to interactions at the population level; more accurate doseresponse functions will be necessary for successful development of such models (see below). The efficiency of a particular resistance trait can be influenced by other plant traits. For example, the alkaloid negatively influences the performance of Heliothis-larvae when incorporated into artificial larval diet (Campbell and Duffy 1979). However, in actual plant tissue the effect is ameliorated by rutin, another secondary metabolite naturally occurring in tomato leaves (Duffy et al. 1986). Thus, to what extent a resistance trait will affect the insect may depend on interactions with other traits. Little is known about this type of complicated interactions, but it is probable that they are common and important (Stamp and Yang 1996; Simpson and Raubenheimer 2001). It is commonly believed that resistance is maintained through mixtures of secondary compounds (Cates 1996), and it is possible that certain compounds are more important than can be judged from mere measuring their concentration if there is a synergistic interaction with a co-occurring toxicant (Berenbaum 1985). To complicate the matter further, under field conditions resistance mechanisms are often modified by environmental factors, abiotic as well as biotic (see below). The response to a particular resistance trait is not universal among insect individuals within a species (e.g., Hanks and Denno 1994; Glynn and Larsson 2000). The fact that such variation exists should come as no surprise because intraspecific variation in preference or performance is the basis for the evolution of food plant specialization among insect taxa. However, the magnitude with which insect individuals in natural systems vary with respect to their ability to overcome resistance traits is largely unknown. Several examples of local adaptations are documented for herbivorous insects (van Zandt and Mopper 1998), but little straightforward evidence exists linking this to plant resistance traits. There are many examples of so called biotypes that are able to overcome resistance in agricultural system (Via 1990). Thus, when studying plant resistance mechanisms it is essential to control for variation among the insect individuals used, especially in studies on insect species with an endophagous feeding mode because these seem to commonly show local adaptations (van Zandt and Mopper 1998). There can be many reasons why all insect species do not respond to variation in a resistance trait in the same way, as discussed above. Regardless of what causes this variation, the diverse responses make it difficult to make statements about the degree of plant resistance based on single observations of insect responses. A somewhat pessimistic view argues that we are dealing with a myriad of

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idiosyncracies and that it will be difficult, if possible at all, to formulate universal theories (Lawton 2000). A more optimistic view would be that the diversity in interactions can be explained once we better understand how resistance traits vary among plants with different life histories (Coley 1988; Loehle 1988), and to what extent insect life history determines the response to such variation (Mattson et al. 1988; Kause et al. 1999b). For the present, however, we need to be cautious when using insect bioassays to test phytocentric hypotheses such as the carbon/nutrient balance (Bryant et al. 1983) or the growth differentiation balance (Herms and Mattson 1992) hypotheses. 5. INDUCED RESISTANCE In the previous section I did not distinguish between constitutive and induced resistance. In many cases, including the issues discussed above, it may not be so important whether the resistance is of a constitutive or an induced nature. In fact, if the plant always responds with an induced reaction to insect damage, which seems to be the case in at least some systems (Edwards et al. 1986), then from an adapted insect’s point of view the response can be seen as functionally constitutive. The tremendous focus on induced plant responses in recent years, however, calls for a special section on insect-induced resistance. It has long been known that microorganisms induce responses in plants that render them resistant to attack (e.g., Kuc 1982). At least in crop systems there can be a very close interaction between the genomes of the two organisms, the resistance gene in the plant and the virulence gene in the pathogen (e.g., Dangl and Jones 2001). The mechanisms behind plant/pathogen interactions have been identified in great detail. Elicitors in the form of oligosaccharids or proteins delivered by the pathogen trigger receptor molecules in the plant (Ebel and Mithöfer 1998). Various types of biochemical cascades follow in the plant cell upon receptor recognition, frequently, but not always, resulting in the hypersensitive response, a type of programmed cell death (Heath 1998). Signal compounds, such as salicylic acid or jasmonic acid, play important roles in the induction of the cascades (Bostock et al. 2001). Through the action of signal compounds resistance can be systemic, i.e. tissues away from the site of infection may also become resistant to the invading pathogen (Mauch-Mani and Metraux 1998). The study of induced resistance to insects has a much shorter history and has proceeded along somewhat different lines (Karban and Baldwin 1997). Some of the insect-oriented research subscribed early on to the resistance paradigm prevailing in plant pathology (Ryan 1983), but most research on insect-induced resistance took a different approach with a focus on phenotypic responses in the plant often detected by using insect individuals as bioassays (Tallamy and Raupp 1991). It soon became clear that insects induce changes in perennial plants that can last over long periods of time, and thus could act as a density dependent factor in insect population dynamics (Benz 1974; Haukioja 1980). Haukioja and Neuvonen (1987) introduced the terms rapid induced response (RIR) and delayed induced response (DIR), the former having effects on insects in the same generation and the latter in

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future generations. The existence of DIR has been well documented in mountain birch Betula pubescens ssp. czerepanovii against the geometrid Epirrita autumnata (Haukioja et al. 1988), although the magnitude of the resistance effect and the plant traits involved are still not fully understood (Kaitaniemi et al. 1998). Another documented case of DIR is the European larch and the larch bud moth Zeiraphera diniana (Baltensweiler and Fischlin 1988 ). There are a number of systems, however, where extensive damage in one year has not resulted in any increased resistance to insects in the following year (Niemelä et al. 1991; Šmits and Larsson 1999). It seems as if coniferous trees are less prone to induction by folivorous insects than deciduous trees, possibly because of differences in carbon allocation strategies (Tuomi et al. 1988). It should be pointed out, however, that all these examples have evaluated effects by bioassaying insect larvae. It is possible that other insect life stages can be affected by induced changes in the plant. For example, Šmits et al. (2001) estimated that realized fecundity of the geometrid Bupalus piniarius can be reduced by about 50% when females are forced to lay eggs on Scots pine trees totally defoliated by larvae in the previous year. Few systems have been studied with respect to host tree effects on egg production (Leather et al. 1987; Tammaru and Javois 2000). Clearly, more research on this aspect of induction is necessary. The RIR referred to by Haukioja and Neuvonen (1987) is a process that operates on a time scale of weeks rather than years. Most evidence of RIR come from bioassays with insects fed damaged and undamaged plant tissue, from phenotypic measures including accumulation of secondary chemicals, or morphological changes in the tissue close to the damage (Tallamy and Raupp 1991). Insect feeding almost always induce at least some changes in the quality of plant traits, but such responses do not always translate into reduced insect performance, and thereby increased resistance (Agrawal 2000a). One difficulty when interpreting data on induced resistance, and indeed variable resistance in general, is how to interpret small but still statistically significant effects. In a provocative paper Fowler and Lawton (1985) questioned the relevance of induction effects because they may be marginal in comparison with other factors influencing insect populations. The RIR in conifers following attack by bark beetles is especially well studied. Resistance to bark beetles can be both of a constitutive and of an induced type (Raffa and Berryman 1983; Raffa 1991). Recent work on Norway spruce (Picea abies) with simulated bark beetle attack (wounding or inoculation with a phytopathogenic fungus) has shown induction of traumatic resin duct formation and polyphenolic parenchyma cells within weeks of infection (Francheschi et al. 2000; Nagy et al. 2000). Because bark beetle attack was simulated by mechanical wounding and inoculation with a fungus, it is difficult to know to what extent these responses represent resistance against the insect (but see Christiansen and Krokene 1999). But on the other hand, bark beetles, and probably many other insects, carry with them microorganisms that are essential for the insect’s normal development. Thus, it may turn out that many of the plant responses that we presently interpret as insect induced in fact are triggered by the microorganisms that are associated with the insect (cf. Barbosa et al. 1991).

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Rapid induced resistance following bark beetle attack has sometimes been referred to as a hypersensitive response (HR) (Raffa and Berryman 1987). Resistance against other insects with an intimate association with their host plant has also been interpreted as HR (Fernandes 1990; Fernandes and Negreiros 2001). HR as defined in the pathology literature (Heath 1998) is a rapid process resulting in cell death, and the mounting of a defense, within hours after the attack. Because most studies involving insects have been conducted over much longer time scales it is unclear whether the necrotic tissue assumed to be indicative of HR in fact is just that or whether it is a consequence of an attack that failed for other reasons (but cf. Ollerstam et al. 2002). The breakthroughs in molecular biology techniques we have witnessed in recent years offer novel methods to study insect induction at the cellular level. Thus, the time scale in the processes under study is reduced to hours or days rather then weeks or months as in RIR sensu Haukioja and Neuvonen (1987). Sometimes insect damage induces the same genes as other biotic agents (Forslund et al. 2000). However, there are clearly herbivore-specific responses, and these are also different from mechanical wounding (Korth and Dixon 1997; Havill and Raffa 1999; Reymond et al. 2000; Halitschke et al. 2001). However, because adapted insects have evolved ways to cope with induced changes in the plant (Duffey and Stout 1996; Baldwin and Preston 1999) it is not clear to what extent the gene products affect the performance of the insect. In some cases performance is reduced at a statistically significant level (Thaler et al. 2001), but in other cases resistance genes are induced without any measurable effects on the performance of the insect (Stotz et al. 2000). The most powerful way of applying molecular methods on plant/insect interactions is, where it is possible, to use mutants or transformation techniques. By such methods molecular responses have been studied in detail in Arabidopsis thaliana (Reymond et al. 2000; Moran & Thompson 2001; Nielsen et al. 2001). Few similar data exist for woody plants. Most research on transformed woody plants has focused on introducing resistance genes from other plant species and then studying effects on bioassay insects (Leple et al. 1995, Confalonieri et al. 1998, Dowd et al. 1998, Delledonne et al. 2001). It will be interesting to see if transgenic trees, e.g., Populus sp., can be used to study basic tree/insect interactions in a manner similar that now ongoing in Arabidopsis research. 6. ENVIRONMENTAL MODIFICATIONS OF RESISTANCE Plant resistance traits are shaped by environmental factors, biotic as well as abiotic. The traits can be modified both in ways that make the plant less (induced resistance) or more (induced susceptibility) suitable to the insect (Karban and Baldwin 1997; Koricheva et al. 1998b) (Fig. 3). Further, tree genotypes may respond differently to a particular environmental factor, in which case we talk about a plastic response, or a genotype by environmental (g x e) interaction. Phenotypic plasticity with respect to plant resistance to insects is probably common (Smith 1989; Cronin and

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Abrahamson 1999), but few data exist on woody plants (Quiring and Butterworth 1994; Orians and Fritz 1995; Björkman 2000).

Certainly the most studied biotic modification of plant resistance is when it is the product of the attacking insect itself. This was covered in the previous section and will not be further discussed. But other organisms can also alter plant characteristics to the extent that the plant becomes more or less resistant to a particular insect (Agrawal et al. 1999a). Recently, the concept of “cross talking” has been introduced in the molecular literature to describe a situation where, for example, a fungus or bacteria elicit plant responses that also lead to induction of resistance to an insect (Felton et al. 1999; Paul et al. 2000; Bostock et al. 2001). Ecologists have frequently observed induction of resistance or susceptibility when a tree has been attacked by other organisms (Danell and Huss-Danell 1985; Faeth 1986; Hatcher et al. 1994; Wallin and Raffa 2001). It is unclear, however, to what extent such phenomena can be explained by cross talk (Hunter 2000).

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The fact that insect outbreaks often occur in stands that seemingly are abiotically stressed has led many to speculate that trees in such stands are less resistant than in non-stressed stands (Rudnew 1963; White 1974; Bombosch and Lunderstädt 1975; Rhoades 1979). Many putative resistance traits are modified by environmental factors (White 1984, Koricheva et al. 1998a), and this has been claimed to be supportive evidence for the stress hypothesis. The stressed-tree explanation for outbreaks requires that the insect can take advantage of stress-induced changes in the tree. This does seem to be the case for certain insect types, i.e. bark beetles and phloem feeders (Larsson 1989; Koricheva et al. 1998b), but for the most part few experimental data exist to support the notion that insects are favored by feeding on stressed plant tissue (Koricheva et al. 1998b). In fact, some insects do respond negatively to stressed plants (Koricheva et al. 1998b) which has led Price (1991) to postulate the opposite, namely that insect performance is enhanced on vigorously growing plants, or plant parts. It may be dangerous, however, to completely reject the plant stress – insect performance hypothesis because in natural forests stressful conditions build up gradually in ways that are poorly understood making proper experimentation difficult (cf. Brown et al. 2001). Also, because stress experiments only rarely control for tree genotype it is possible that treatment effects have been difficult to detect if trees show phenotypic plasticity with respect to stress responses. The underlying observation, i.e., that outbreaks frequently correlate to seemingly stressful abiotic conditions, cannot be ignored but perhaps explanations based on tree resistance alone are simplistic (Larsson et al. 1993). 7. RESISTANCE IN THE CONTEXT OF COMPLEX INTERACTIONS In natural systems, plant resistance is one of many selective agents affecting herbivore fitness. It is particularly important to recognize that effects of plant resistance traits on insect growth and survival can be much modified by natural enemies, i.e., tri-trophic level effects (Price et al. 1980; Agrawal 2000b). Many plant traits, seemingly with a defensive function, do not cause mortality in feeding insects, although insect growth rate may be reduced. When studied in the laboratory such sub-lethal effects can in fact lead to more damage to the plant because the insect compensates by consuming more leaf tissue (e.g., Docherty et al. 1996). Possibly, this “paradox of sub-lethal plant defense” (Moran and Hamilton 1980) can be resolved by taking into account higher trophic levels; insects feeding on resistant plants, resulting in longer development time, are more exposed to natural enemies, and thus, may suffer higher predation mortality compared to conspecifics feeding on susceptible plants (Häggström and Larsson 1995; also cf. Agrawal et al. 1999b). Because natural enemies are significant mortality agents in most insect herbivore populations (Cornell and Hawkins 1995), it is necessary to consider this interaction whenever sub-lethal effects are present (Kondoh and Williams 2001). Unfortunately, it is difficult to analyze because natural enemy population density varies spatially and temporally in ways that are most often unknown, and thus the extent to which "slow growth-high mortality" is a significant

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modifier of insect-caused plant damage in a particular environment will be difficult to predict (cf. Gratton and Welter 1999). In certain interactions the insect has not only evolved mechanisms to cope with plant secondary metabolites but has taken advantage of their toxic properties for use in defense against its enemies (Rowell-Rahier and Pasteels 1992). This type of defense probably offers a considerable fitness gain, and thus could have been an important factor in the evolution of host plant specialization in herbivorous insects (Bernays and Graham 1988). For example, larvae of the leaf beetle Phratora vitellinae suffer higher mortality from generalist predators when forced to feed on willow leaves lacking salicin, the precursor of its anti-predator defense, than larvae fed leaves of its normal host that contain salicin (Denno et al. 1990). Many interactions of this kind have been described (Rowell-Rahier and Pasteels 1992). Thus, when the plant interacts with these highly specialized insects the secondary metabolite cannot, by definition, be considered a resistance trait because insect fitness is enhanced rather than reduced. When considering a plant trait such as salicin it is important, therefore, to be explicit in the formulation of the research question. A plant-oriented hypothesis, for example whether or not there is a cost associated with producing salicin, needs to be specified according to expected benefits. In the case of P. vitellinae there are seemingly small, if any, benefits for the plant to contain salicin. However, less specialized insects do suffer reduced performance by ingesting leaf tissue that contains salicin (Hodkinson et al. 1998). A very special kind of induced resistance is when the plant "calls for help" from natural enemies, i.e. the damage caused by the herbivore results in the release of novel volatile compounds that attract natural enemies (Dicke 1999; Farmer 2001). This "indirect defense" (Baldwin and Preston 1999) involving the third trophic level has been intensively studied in recent years. Most well-studied examples include attraction of parasitic wasps to plant tissue damaged by caterpillar feeding (Turlings et al. 1995). It is not clear to what extent the plant really benefits from this interaction because most parasitized larvae continue to feed at least as much and sometimes more than non-parasitized larvae (van der Meijden and Klinkhamer 2000). If predators also were attracted, then induction clearly would be adaptive because increased predation mortality would lead to reduced damage to the plant. A recent study has indeed found generalist predators to respond to volatiles induced in Nicotiana attenuata leaves following damage by three species of leaf-feeding herbivores (Kessler and Baldwin 2001). Still, it is possible that volatile induction is simply a by-product of feeding when caterpillar saliva is mixed with the plant cell content. An interesting alternative, albeit not mutually exclusive, explanation is that the volatiles are produced primarily for the benefit of the herbivore, for example, by acting as deterrents for egg-laying females and thereby reducing competition among conspecific larvae (De Moraes et al. 2001; Kessler and Baldwin 2001). Most detailed studies on herbivore-induced volatile emission are from herbs or grasses (Dicke 1999; Dicke and Bruin 2001). Volatiles were implicated as a possible underlying mechanism in the "talking trees" studied during the 80's (Baldwin and Schultz 1982; Rhoades 1983); however, interpretations of these experiments are problematic. Havill and Raffa (2000) recently found increased parasitoid attraction

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to volatiles from poplar leaves damaged by gypsy moth larvae, compared to nondamaged leaves (also cf. Dolch and Tscharntke 2000; Tscharntke et al. 2001). Thus, it seems reasonable that future studies on trees, based on the same protocols as used with herbs and grasses, will document volatile induction also in woody plants. 8. RESISTANCE AND INSECT POPULATION DYNAMICS Time scale is an essential component for assessments of the "importance" of plant resistance to insects. When testing hypotheses on an evolutionary time scale, it may be appropriate to ask, for example, whether or not differences in resistance among plant genotypes lead to statistically significant variation in insect fitness. If so, then there is potential for plant traits to influence the evolution of insect life history traits. However, when examining processes on an ecological time scale, the magnitude of the effect, not only statistical significance, needs to be taken into account (Fowler and Lawton 1985; Kytö et al. 1996). For example, whether or not variation in a particular resistance trait can account for ups or downs in insect numbers needs to be examined in the context of other factors influencing the performance of the insect, in particular, density dependent factors that may overshadow any effects that plant traits have on the performance of insect individuals (Hunter 1997). Few systems have been examined in enough detail to allow such analyses. The natural variation in the expression of the resistance trait, responses of insect individuals to the full range of plant resistance variation, the magnitude of other factors acting on insect individuals, and the behavior of density dependent factors are most often not all known for any single system. For the European pine sawfly Neodiprion sertifer reasonably good data exist on larval responses to variable needle terpenoid (resin acid) concentrations (Larsson et al. 1993), and there is good reason to assume that cocoon predation by small mammals is the most important density dependent mortality factor (Hanski 1990). Larval survival and sawfly fecundity are reduced at high resin acid concentrations (Larsson et al. 1986). However, high resin acid concentrations are, at the same time, beneficial because larval defense against predators is enhanced (Björkman and Larsson 1991); thus, the pine/sawfly system is a case where tri-trophic interactions are potentially important. These observations formed the basis for the development of a simple population model to evaluate the importance of variable needle resin acid concentrations for the onset of sawfly outbreaks (Larsson et al. 2000). In the model, data on individual responses were combined with literature data about cocoon predation at the population level. The analysis showed that the probability of plant-mediated escape from natural-enemy control, i.e., risk for an outbreak, is high when needle resin acid concentration (r) or larval predation pressure (p) is low, and by analyzing different scenarios it was found that small changes in r and p can result in the sawfly population moving from low to high outbreak risk (Fig. 4). In the sawfly model, one resistance trait, concentration of needle resin acids, was examined. In a natural situation, plant traits interact and the sum of their effect on performance of insect individuals is complex (Duffey and Stout 1996). Nevertheless, formal analyses including processes both at the levels of the

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individual and the population are urgently needed before anything can be said about the "importance" of plant resistance traits for the dynamics of insect populations.

One serious complication is that the temporal and spatial variation in traits of importance for insect performance is unknown for the great majority of tree species. Still, in order for plant traits to contribute to insect population dynamics one has to assume variation in trait quantity, and thus effects on the performance of insect individuals. With regard to the onset of insect outbreaks abiotic stress has been implicated as the factor that induces changes in trait quantity, e.g., increased concentrations of soluble amino acids (White 1974) or decreased concentrations of secondary metabolites (Rhoades 1979). Unfortunately, data from forest stands suitable to test this hypothesis are difficult to collect, and experimental data are inconclusive (Koricheva et al. 1998b). Future research efforts will have to combine

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a multitude of approaches, including long-term monitoring of plant and insect, manipulative experiments, and modeling in order to successfully address hypotheses involving the importance of tree resistance at the population level. ACKNOWLEDGMENTS I thank Christer Björkman, Erik Christiansen, Barbara Ekbom, Bob Fritz, Julia Koricheva, and Tim Paine for helpful comments on earlier drafts of this chapter. Financial support was provided by the Swedish Council of Forestry and Agricultural Research (SJFR), and the Royal Swedish Academy of Agriculture and Forestry (KSLA).

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Turlings, T.C.J., J.H. Loughrin, P.J. McCall, U.S.R. Röse, W.J. Lewis, & J.H. Tumlinson, 1995. How caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proceedings of the National Academy of Sciences of the USA 92:4169-4174. van Dam, N.M., & J.D. Hare, 1998. Differences in distribution and performance of two sap-sucking herbivores on glandular and non-glandular Datura wrightii. Ecological Entomology 23:22-32. van der Meijden, E., & P.G. Klinkhamer, 2000. Conflicting interests of plants and the natural enemies of herbivores. Oikos 89:202-208. van Zandt, P.A., & S. Mopper, 1998. A meta-analysis of adaptive deme formation in phytophagous insect populations. American Naturalist 152:595-604. Via, S., 1990. Ecological genetics and host adaptation in herbivorous insects: The experimental study of evolution in natural and agricultural systems. Annual Review of Entomology 35:421-446. Wagner, M.R., & Z.I. Zhang, 1993. Host plant traits associated with resistance of ponderosa pine to the sawfly, Neodiprion fulviceps. Canadian Journal of Forestry Research 23:839-845. Wait, D.A., C.G. Jones, & J.S. Coleman. 1998. Effects of nitrogen fertilization on leaf chemistry and beetle feeding are mediated by leaf development. Oikos 82:502-514. Wallin, F., & K.F. Raffa, 2001. Effects of folivory on subcortical plant defenses: can defense theories predict interguild processes? Ecology 82:1387-1400. Waring, R.H., & G.B. Pitman, 1985. Modifying lodgepole pine stands to change susceptibility to mountain pine beetle attack. Ecology 66:889-97. Watt, A.D., & I.P. Woiwod, 1999. The effect of phenological asynchrony on population dynamics: analysis of fluctuations of British macrolepidoptera. Oikos 87:411-416. Werker, E., 2000. Trichome diversity and development. Advances in Botanical Research 31:1-35. White, T.C.R., 1974. A hypothesis to explain outbreaks of looper caterpillars, with special reference to populations of Selidosema suavis in a plantation of Pinus radiata in New Zealand. Oecologia 16:279301 White, T.C.R., 1984. The abundance of invertebrate herbivores in relation to the availability of nitrogen in stressed food plants. Oecologia 63:90-105. Winterer, J., & J. Bergelson. 2001. Diamondback moth compensatory consumption of protease inhibitor-transformed plants. Molecular Ecology 10:1069-1074. Yukawa, J., 2000. Synchronization of gallers with host plant phenology. Population Ecology 42:105113. Zangerl, A.R., & M.R. Berenbaum, 1993. Plant chemistry, insect adaptations to plant chemistry, and host plant utilisation patterns. Ecology 74:47-54. Zvereva, E.L., M.V. Kozlov, & P. Niemelä, 1998. Effects of leaf pubescence in Salix borealis on host plant choice and feeding behaviour of the leaf beetle, Melasoma lapponica. Entomologi Experimenta l is et Applicata 89:297-303.

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CHAPTER 2 MECHANISMS OF RESISTANCE IN CONIFERS AND BARK BEETLE ATTACK STRATEGIES

FRANÇOIS LIEUTIER Université d’Orléans, Laboratoire de Biologie des Ligneux et des Grandes Cultures B.P. 6759, F.-45067 Orléans Cedex, France. and : INRA, Unité de Zoologie Forestière BP 20619 Ardon, F-45166 Olivet Cedex, France.

1. INTRODUCTION Bark beetles are the most damaging pests of coniferous forests worldwide. It is well established that the key-factor in their population dynamics is food quantity, or the number of host trees in a condition that makes them susceptible to successful colonization. The role of the host is central in all aspects of the bark beetle life cycle. As with any other living organism, trees are able to defend themselves against attacks and, during the colonization process the beetles must overcome various resistance mechanisms. Host resistance is absent in freshly felled trees that are always successfully colonized and thus represent an easily accessible source of food. It can reach very high levels in healthy and vigorously growing trees that are unsuitable for beetle establishment and thus are an inaccessible source of food. The quantity of food available for the beetle population directly depends on the efficiency of the tree’s resistance mechanisms, which are thus the real key-factor of bark beetle population dynamics for species that attack living trees. Consequently, it is not surprising that the study of the relationships between bark beetles, their associated phytopathogenic fungi and their host tree, especially its resistance, has led to dramatic improvements in knowledge about bark beetle biology and population dynamics. Here, I present an overview of the state of the art in this field, emphasizing advances in knowledge during the last 5 years. I will consider only the mechanisms themselves, not their variations with genetic and/or environmental factors. First, the different defense systems involved in resistance of conifers to bark beetles will be covered. Next, I will describe how trees resist attacks, the mechanisms involved, and the respective roles of the defense systems. 31 M.R. Wagner et al. (eds.), Mechanisms and Deployment of Resistance in Trees to Insects, 31–77. © 2002 Kluwer Academic Publishers. Printed in the Netherlands.

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Then, I will consider how beetles overcome the resistance of the trees including the mechanisms of attack and establishment and the different colonization strategies that beetles use. Conclusions will focus on research prospects and potential application of resistance to bark beetles. 2. LEVELS OF TREE RESISTANCE According to Karban and Baldwin (1997), resistance must be distinguished from defense. Resistance is considered from the beetle’s perspective and refers to the difficulty of establishing in the host, whereas defense refers to the host facing the beetles. These may or may not be the same thing. Moreover, defense often supposes an active mechanism (particularly in response to aggression), while resistance can also include passive non-induced phenomena. There are 2 main types of resistance in plants facing attack by living organisms. Preformed resistance mechanisms exist in the absence of attack by the beetles. There is no gene activation and transcription control resulting in increased synthesis following damage. The plant has invested resources in defense before damage occurred (preformed defenses). Induced resistance mechanisms are “turned on” only when beetles attack the tree. Genes are activated by the damage, resulting in increased synthesis of specific compounds. The plant invests resources in defense after damage has begun (induced defenses). I summarize the main types of defenses (preformed and induced) occurring in conifers subjected to bark beetle attacks and their potential role in host resistance in the sections that follow. For convenience, these mechanisms are presented separately but they are not independent constituents of tree resistance. They develop simultaneously and complement each other, even if their effects on the beetles do not occur at the same time. 2.1 PREFORMED DEFENSES The cells responsible for the syntheses of the defensive chemicals involved in preformed defenses are secretory structures already specialized in that function. There is no change in the metabolism of the secretory cells, which are generally localized, in well-defined tissues. These structures are present in any tree organ and are responsible for the first line of resistance met by the invaders (beetles and eventually fungi). There are, however, two possibilities in preformed resistance (Karban and Balwin, 1997). When the defensive structures are active in the same state as they were before aggression, they correspond to the “constitutive resistance” or “constitutive defense”. When they need to be activated to play a role in resistance, either because a wound is necessary to release an active compound or because an inactive precursory compound becomes active after being released by a wound, they correspond to the “activated defense” or “preformed induced defense”. 2.1.1. Constitutive defense Bark thickness can be an efficient constitutive defense against bark beetle species that usually attack the upper parts of the trees, such as Pityogenes chalcographus on

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spruce and Ips acuminatus on pine in Europe. Lignin located in the outer bark and the phloem of various conifer species is often concentrated in numerous patches disseminated in the tree tissues (Figure 1). These structures, sometimes called “stone cell masses”, are inevitably met by the beetles when boring their galleries, and their hardness can dissuade the beetles from continuing the attack if they are abundant, as in the case of Dendroctonus micans in Norway spruce (Wainhouse et al., 1990, 1998).

Nevertheless, although absolutely passive, this constitutive defense may influence the development of induced mechanisms. In Norway and Sitka spruces, a negative correlation was found between the size of the lesions induced by artificial inoculations of fungi and the concentration of the lignified stone cell masses in the phloem (Wainhouse et al., 1997). This interaction between such distinct defense systems illustrates the complementarity and interdependence of the mechanisms involved in the various kinds of defense. 2.1.2. Preformed induced defense Two main anatomical systems in conifers are sites for storage of secondary metabolites that are released or become active after wounding by aggressors. Blisters and resin ducts store monoterpenes and resin acids (Johnson and Croteau, 1987), while specialized phloem parenchyma cells store soluble phenols as well as more complex polyphenolic compounds (Franceschi et al., 1998). Resin ducts form an elaborated resin system in the genera Pinus, Picea, Larix and Pseudotsuga, which do not possess blisters (Bannan, 1936). Vertical and radial ducts are connected to each other and resin is synthesized by secretory cells lining these ducts (Bannan, 1936; Shrimpton, 1978) (Figure 2). Vertical ducts are the most abundant and are located in the sapwood only, while radial ducts occur in both the sapwood and the phloem. There is contiguity between the sapwood radial ducts and those of the phloem but usually no communication exists between them (Shrimpton, 1978). However, communications exist between the vertical and radial ducts of the sapwood. Consequently, the main location of the resin duct system is sapwood and the amount of resin flow exuded by a wound has been correlated with the density of

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vertical resin ducts (Blanche et al., 1992) which represent the most important reservoir of preformed

resin in conifer species that have resin ducts. The beetles cut resin ducts in the phloem and superficial sapwood when they bore their galleries. When galleries do not sever the sapwood, trees respond to the wound by creating continuity between the sapwood and phloem radial ducts (Gambliel et al., 1985), thus allowing the mobilization of the sapwood reservoir. The resin flow released by slashing of the duct system is thus typically a preformed induced defense. Indeed, resin is synthesized before aggressions but requires damage to tissues and building of a communication between phloem and sapwood to be released and to get in contact with the aggressors. This resin flow involves the rapid transport of chemicals to the site of damage. In fact, although no induced synthesis is involved in it, the preformed resin flow is often mixed with the induced resin flow and the resin exuding from the saturated tissues involved in the hypersensitive response (see below). The direction of gallery boring is important for this kind of defense system to play a significant role in tree resistance (Berryman, 1972; Lieutier, 1992). Because of the organization of the resin duct system, vertical galleries are sectioning both vertical and radial ducts at the beginning of the beetle tunnelling activity, but only radial ducts later on. Since the vertical ducts are the most abundant, the effect of resin flow in that case is mostly limited to the moment of gallery initiation. On the other hand, horizontal galleries cut both vertical and radial ducts during the whole tunnelling activity, which gives the resin flow a greater chance to play a role, as demonstrated for D. micans in Picea abies (Lieutier et al., 1992). Moreover, the chance for this defense system to counteract beetle attacks is especially high in tree species (mostly pines) where the resin network is particularly developed and for those that are able to rapidly exude large quantities of resin. Among pines, however, geographic or between species differences exist. The preformed resin flow is presumed to be the main defense system against D. frontalis in several pine species in the southern United States. Interspecific variation in its characteristics would also

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explain why different tree species in this area diverge in their susceptibility to attack (Hodges et al., 1979; Matson and Hain, 1985; Nebeker et al., 1988, 1993). It has a much more limited impact against D. ponderosae in lodgepole pine (Pinus contorta) in the north-western US (Raffa and Berryman, 1982a) and against Ips and Tomicus species in Scots pine (Pinus sylvestris) in Europe (Lieutier et al., 1988, 1995; Schroeder, 1990). Spruces have a limited resin flow as observed in Norway spruce (Picea abies) during I. typographies attacks (Christiansen and Horntvedt, 1983; Christiansen, 1985a). Blisters are cavities mainly located in the outer bark of Abies, Tsuga and Cedrus, which do not possess resin ducts (Bannan, 1936). In these species, large quantities of resin exude when blisters are damaged and could play a role in arresting the aggressors. However, beetles apparently avoid these resin pockets while attacking a tree, as demonstrated for Scolytus ventralis in Abies concolor (Ferrell, 1983). The role of resin flow is wound cleansing by flushing the wounded tissues and then sealing the wound through resin crystallization (Berryman, 1972; Nebeker et al., 1995). It can also have a physical effect on the aggressors through flushing, viscosity and crystallization rate; oleoresin exudation pressure has been reported to be correlated with tree resistance (Vite 1961; Cates and Alexander, 1982). In addition, a chemical effect obviously exists since terpenes from preformed resin can be repellent or toxic for the beetles and their associated micro-organisms (Reid and Gates, 1970; Raffa et al., 1985; Paine and Hanlon, 1994; Raffa and Smalley, 1995). However, fungi can often tolerate the preformed resin flow (Cobb et al., 1968; Shrimpton and Whitney, 1968), as do many beetles that are able to swim in it. On the other hand, this resin flow dries up very rapidly (Nebeker et al., 1992; Raffa and Berryman, 1983a). Moreover, when the flow is efficient, beetles often can escape. Then, owing to the high variability of the resin flow within a tree (Schroeder, 1990), they can succeed in initiating a gallery elsewhere in the same tree, thus circumventing this defense system (Lieutier et al., 1995). When effective however, in addition to its physical and direct chemical effects, the constitutive resin flow can interfere with pheromone emission and thus stop beetle aggregation (Raffa and Berryman, 1983a). The polyphenolic parenchyma cells (PP cells) of conifers are located in the phloem where they represent the second numerically important cell category, after the sieve cells. They are organized mainly in concentric parallel rows all around the tree with one row per year (Franceschi et al., 1998; Krekling et al., 2000) (Figure 3). As the tree is enlarging, additional PP cells can be produced in

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the already existing rows, by differentiation of axial parenchyma cells or by division of already differentiated PP cells, thus forming permanently continuous layers of cells (Krekling et al., 2000). This particular organization inevitably results in the destruction of many PP cells and rows when a beetle bores a gallery or when its associated fungus invades the phloem. Under such wounding conditions, large quantities of phenolics previously stored in the PP cells can be released (Franceschi et al., 1998). The assumption that these cells contribute to the tree’s preformed defense is based on the observation that, in Norway spruce, their density is much higher in resistant than in susceptible trees and their content also seems to be in a more soluble form in resistant trees (Franceschi et al., 1998). This is of interest since it has been demonstrated that resistance in Norway spruce clones is correlated with the content of their phloem in certain soluble phenols before any aggression (Brignolas et al., 1998). However, we still have no direct demonstration of the effectiveness of this preformed defense system, although phenols are known to have antifungal properties and to be feeding deterrents for phytophagous insects (Nicholson and Hammerschmidt, 1992; Appel, 1993). 2.2. INDUCED DEFENSES These defenses are considered as plant responses, and are typically categorized as short term or long-term inducible responses or mechanisms (Mattson et al., 1988). Another classification uses the complexity of the changes occurring in the cells involved in the tree response (Franceschi et al., 2000). Limited changes in the metabolism of cells already specialized in the same function before aggression would be at one end of the ranking, while complex changes involving cell division and differentiation would be at the other end. Presently these two classification systems overlap closely in regard to tree responses to bark beetles, since limited changes are associated with short term responses while complex changes occur under long term responses. The three main steps in these classification systems are induced resin flow, hypersensitive reaction, and delayed resistance. Each step corresponds to a particular kind of induced defense.

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2.2.1. Induced resin flow Ruel et al. (1998) recently described this type of induced defense in loblolly pine (P. taeda) in the southern U.S. Trees were wounded repeatedly over several days, while measuring the resin flow periodically (Figure 4). After a rapid (24 hours) drying up of the preformed resin flow, a new resin flow appeared in two days and increased

during the following days, reaching 2 -3 times the values of the preformed flow in five days. Such a considerable and rapid increase of the resin flow cannot be explained by a simple refilling of the ducts. At least a large-scale resin translocation was involved. However, according to the authors, large-scale translocations are unlikely to occur in pines because resin ducts in these trees do not form a true network. Moreover, this would require a decrease of resin flow in other parts of the tree. Thus, although not yet proved, it was concluded that the new resin flow was a reaction of the tree induced by the wounds and not specifically linked to the stimulus. Induced resin flow appears only after preformed resin flow (preformed induced defense) has stopped. Similarly, the classical hypersensitive reaction also is not specific and exists after repeated wounding but it is less rapid. Another difference compared to the hypersensitive reaction is the category of cells responsible for syntheses of the induced resin. Indeed, the cells involved in induced resin flow are very likely those that are already responsible for the synthesis of preformed resin, while those involved in resin synthesis of the hypersensitive reaction differ completely (see below). Induced resin flow would thus correspond simply to a stimulation of the metabolism of cells already specialized in the same function, which would explain the rapidity of the response. However, until a study of the chemical composition of induced resin flow is carried out, it is impossible to know if this stimulation is accompanied by modifications of cell metabolism. Certainly induced resin flow can stop beetle boring and thus extend the role of the preformed resin flow. It can also play a role in perturbing pheromone emission and thus stopping beetle aggregation. However, nothing can be concluded regarding

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a possible chemical effect since its chemical composition is still unknown. The resistance mechanism of preformed resin flow is certainly more efficient in pines than in other conifers. It may be significant that it has been discovered in loblolly pine. 2.2.2. Hypersensitive reaction Reid et al. (1967) first described the hypersensitive reaction induced by a bark beetle attack in conifers and presented the role of the fungi associated with the beetles in amplifying the reaction mechanisms. They suggested that this so-called “secondary” reaction (as opposed to “primary” preformed resin flow) plays the most important role in conifer resistance to bark beetles. Berryman (1972) generalized these ideas and presented the first synthetic hypothesis of tree resistance and beetle success taking into account the tree’s hypersensitive reaction. Berryman (1976) proposed a model of bark beetle population dynamics taking the tree resistance mechanisms into account. Subsequently, a considerable amount of research has been developed in this field, and the hypersensitive reaction has been demonstrated to play a basic role in the resistance of many conifer species to many bark beetles species and their associated fungi (Safranyik et al., 1975; Raffa and Berryman, 1982a,b; Christiansen et al., 1987; Raffa, 1991; Paine et al., 1997). However, Nebeker et al. (1993) reported it plays only a minor role against pine bark beetles in the southern U.S.

This tree reaction develops around each point of aggression, in both the phloem and the sapwood. It is visible as a longitudinal resin impregnated zone associated with extended cell necrosis (Reid et al., 1967; Berryman, 1969, 1972; Lieutier and Berryman, 1988a; among others) (Figure 5). The zone is considerably enriched with terpene and neosynthesized phenolic compounds and impoverished with sugars (Shrimpton, 1973 and see section III.2 below). The synthesized compounds invade

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intercellular spaces and sieve cells, thus leading to the death of the affected tissues (Lieutier and Berryman, 1988a). The reaction develops at a distance, ahead of the area infested by the insects and their associated fungi. In the phloem of Norway spruce, intercellular communications exist between the PP cells and the ray parenchyma cells, which are highly interconnected to each other through plasmodesmata. These connections could be the way the signal for the response is transmitted at a distance from the aggressor (Krekling et al., 2000). The reaction acts both physically and chemically against the aggressors in addition to depriving them of nutrients (see below). In resistant trees, these physical and chemical changes in tree tissues contribute to stop fungal growth (fungistatic effect) and prevent gallery construction and oviposition by the beetle (Reid et al., 1967; Berryman, 1969 and see below). Chemical, histological, anatomical and cell studies have revealed that the hypersensitive reaction is a wound reaction induced by the mechanical stress caused by the tunnelling activity of the beetle, and that it is not induced by the fungi introduced by the beetle in its gallery (Lieutier et al., 1988, 1995; Franceschi et al. 1998). However, the reaction can be considerably stimulated and amplified when a fungus is present in the beetle gallery (Lieutier et al. 1988, 1995). Raffa and Smalley (1995) suggested that both structural and metabolic properties of the fungi are important because an inoculation with an autoclaved unviable fungus induced a reaction with an intensity intermediate between that induced by an aseptic wound and that induced by a living fungus. Because of the role of wounding in the induction, the direction of the beetle gallery is certainly important for the development of the reaction. Indeed, due to the anatomical structure of the tree, the hypersensitive reaction develops naturally mainly in the longitudinal direction. Consequently, it is strongly stimulated by longitudinal beetle galleries. The induction by wounding and the amplification by the fungi associated with the beetles had been mentioned by Reid et al. (1967), Wong and Berryman (1977), Raffa and Smalley (1995) and others, but without assigning specific roles to the beetle tunnelling activity and the fungi. Lewinsohn et al. (199la, b) suggested that pines do not respond to mechanical wounding by increasing synthesis of resin but rather use translocation in resin ducts, which means that there would be no hypersensitive reaction after wounding. However, the chemical composition of tree tissues in the reaction zone of the hypersensitive reaction, differs greatly from that in the unwounded tissues in both terpenes and phenolic compounds, even after wounding alone (Russel and Berryman, 1976; Raffa and Berryman, 1982b; Gambliel et al., 1985; Paine et al., 1987; Delorme and Lieutier, 1990; Lieutier et al., 1991a; Brignolas et al., 1995a; Bois and Lieutier, 1997). This would not be possible if only translocation of resin occurred. Moreover, gene activation (Chiron et al., 2000) and neosyntheses with increased enzyme activities (Brignolas et al., 1995b) have also been demonstrated to occur after wounding. In addition, the cytological modifications observed after wounding in the PP cells involved in phenol syntheses, are the same as those observed after a biotic aggression (Franceschi et al., 1998). Although the rapidity and the extension of the hypersensitive reaction depend on the aggressor, the patterns of response development, as well as the associated qualitative (chemical, anatomical or histological) changes are identical in a tree,

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whatever the aggressor (different fungi, different beetles, or wounding). This nonspecific response to various aggressors was observed by Reid et al. (1967) and Wong and Berryman (1977) through similarities of the tree’s response to wounding and fungus aggression, but they did not specifically mention it. It has now been clearly demonstrated at the chemical level through analyses of the monoterpene and phenol contents of the phloem reaction zones, in various conifer species (Cook and Hain, 1985; Delorme and Lieutier, 1990; Lieutier et al., 1991b; Raffa and Smalley, 1995; Popp et al., 1995; Brignolas et al., 1995a; Bois and Lieutier, 1997) and at the histological level (Lieutier and Berryman, 1988a; Franceschi et al., 1998). Changes in the nature of the aggressor elicit only quantitative variations in the tree’s hypersensitive response. Metabolic modifications associated with the hypersensitive reaction are much more extended than those involved with induced resin flow. Specialized phloem parenchyma cells, without relation to the cells involved in the synthesis of the preformed resin, are responsible for induced delocalized syntheses of terpenes (Cheniclet et al., 1988; Lieutier et al., 1988). The same PP cells involved in the preformed defense seem to be responsible for the neosyntheses of phenolics (Franceschi et al., 1998), although heavy changes occur in their metabolism (Brignolas et al., 1995b; Chiron et al., 2000). However, no changes in cell division and differentiation seem to be associated with this reaction. Because the hypersensitive reaction is a wound reaction not specifically linked to the stimulus, it is logical to hypothesize that the elicitors involved originate from the tree itself and not from the aggressors (Wong and Berryman, 1977; Berryman, 1988; Lieutier and Berryman, 1988; Lieutier, 1993). A simple working diagram of these mechanisms has already been proposed (Figure 6, and Lieutier, 1993), taking into account these particularities, the relationships between the hypersensitive reaction and the aggressors, and the possible role of the wound periderm (see below).

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The hypersensitive reaction is completed by the formation of a wound periderm containing an impervious cell layer which develops after the aggressors have been stopped or at least considerably slowed down (Reid et al., 1967, Müllick, 1977; Wong and Berryman, 1977; Berryman and Ferrell, 1988; Lieutier et al. 1990, 1993), while traumatic resin ducts are built up in the sapwood that closely surrounds the reaction (Safranyik et al., 1988). This is the final step of the reaction, which leads to the isolation of the reaction zone (dead tissues) from the rest of the tree, in a compartmentalization process (Shigo, 1984). In fact, according to the criteria of the classification system presented above, the formation of the wound periderm is a long-term induced response since it involves changes in cell division and differentiation (see below). 2.2.3. Delayed resistance This type of induced defense concerns long term inducible responses with complex changes involving cell division and differentiation. Two kinds of resistance mechanisms are associated with bark beetle attacks – the wound periderm and the induced protection phenomenon. Development of wound periderm has been studied in detail by Müllick (1977) with different aggressors such as the balsam woolly adelgid (Adelges piceae [Ratzeburg]) and various pathogens and wounds. Development of wound periderm was covered in the previous section in relation to attacks by bark beetles and their associated fungi. It is mainly involved in the wound healing processes after the hypersensitive reaction is terminated and is thus not a real defense mechanism.

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Nonetheless, wound periderm is worth mentioning because it may contribute to limiting further extension of fungus. From his histological studies, Müllick (1977) concluded that it is basically a wound reaction oriented towards tissue restoration, and not specifically linked to a stimulus.

The phenomenon of induced protection has been recently discovered and described in P. abies regarding artificial mass inoculations with Ophiostoma polonica, a pathogenic fungus associated with Ips typographus (Christiansen et al., 1999a; Krokene et al., 1999). When the boles of Norway spruce trees were pretreated with mass inoculations of fungus at below the lethal density, they became resistant to mass inoculations made three weeks later in the same zone of the tree with the same fungus but at a deadly dosage (Figure 7). Trees pretreated with malt agar alone also exhibited increased resistance to further mass inoculations, although at a lower level than that of trees pretreated with the fungus. This induced protection has been hypothesized to be related to building of traumatic resin ducts around the wounds, although they have not been observed in the same experiment and their role in the increase of resistance not been demonstrated directly (Krokene et al., 1999). Indeed, in the same tree species, traumatic resin ducts appeared locally at wound sites at least two weeks after wounding (Christiansen et al., 1999b; Nagy et al., 2000). This is the same delay at which the induced protection was observed in the experiment reported above, and it seemed to be more developed in resistant compared to susceptible clones (Nagy et al., 2000). Traumatic resin ducts have often been observed in trees surviving beetle attacks or fungal infection (Berryman, 1969; Christiansen and Solheim, 1990; Kyto et al., 1996). They have even been observed at a distance of several meters one year after wounding (Christiansen et al., 1999b). Reid et al. (1967) also reported the existence of traumatic resin ducts after

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one year at 3-4 feet from the wound in pines. These observations are very similar to what has been observed in the leader shoot of white spruce (Picea glauca) attacked by Pissodes strobi (Alfaro, 1995; Alfaro et al., 1996). Regarding bark beetle population dynamics, the build-up of induced protection could accelerate the collapse of outbreaks by protecting the trees from further attacks (Christiansen et al., 1999b). Indeed, the establishment of a network between the traumatic ducts and the radial ducts would form an important reservoir of resin, which could be rapidly mobilized in case of attacks that sectioned the radial ducts. Under these conditions, if the formation of traumatic resin ducts effectively increases tree resistance, the presence of these ducts at a distance from the wounds may lead to systemic induction of resistance. However, one year after pretreatment, mass inoculations at a distance from the pretreatment zone did not reveal any induced protection, although the protection was still effective in the inoculated zone (Krokene et al., 2000). If the hypothesized role of traumatic resin ducts is accepted, the induced protection phenomenon corresponds effectively to a long term and complex induced reaction involving cell division and differentiation. Alternatively, the fact that trees pretreated with malt agar exhibited the same response, but at a lower level, as those pretreated with the fungus, suggests that the phenomenon is induced by wounding, is not specifically linked to aggressors, and is amplified by the presence of the fungus. This non-specificity has also been observed at the histological level (Franceschi et al., 2000). The same conclusions can be drawn regarding the formation of the traumatic resin ducts. They have been known for a long time to be induced by wounds (Bannan, 1936), they correspond to a non-specific response of the tree, and their formation is stimulated by the presence of the fungus (Tomlin et al., 1998; Christiansen et al., 1999b; Nagy et al., 2000). 3. MECHANISMS OF INDUCED DEFENSE 3.1. INDUCTION AND TREE RESPONSES All the recent results presented above support the following two properties shared by all types of tree defense induced by bark beetle attacks: 1- the role of mechanical wounding in inducing the tree response; 2- the non specificity of the tree response. A third observation concerns the almost generalized and ubiquitous role of the phloem parenchyma cells. 3.1.1. Induction by mechanical wounding I hypothesize that, in all induced defenses in trees that concern bark beetle attacks, mechanical wounding is the initial stimulus that induces the tree’s reaction and that this reaction can be stimulated (amplified and accelerated) when fungi are present in the wound. This is in agreement with the pioneer conclusions by Müllick (1977) for the balsam wooly adelgid in Abies, root rot (Phellinus weirii) in Pseudotsuga menziesii, arid blister rust (Cronartium rubicola) in Pinus monticola regarding the generality of the role of wounding. However, Müllick’s observations did not deal with tree defense but basically with tissue restoration (wound periderm). Moreover,

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only a positive or negative interference of the aggressors with tissue restoration was reported, without mentioning a possible stimulation. Regarding bark beetle attacks, Reid et al. (1967) already mentioned the role of fungi in aggravating and expanding wound effects for attacks on Pinus contorta by Dendroctonus ponderosae, but they did not make conclusions regarding induction, nor did they generalize their observations. In experiments with Scots pine (Pinus sylvestris) submitted to attack by Ips sexdentatus and Tomicus piniperda, Lieutier et al. (1988, 1995) suggested that wounds caused by the tunnelling activity of the beetles induced a hypersensitive reaction which was eventually completed by an amplification of the tree response by the fungi. Lieutier (1993) generalized this cause-and-effect relationship to all interactions among conifers, bark beetles, and fungi . It also seems possible to extend these conclusions to delayed induced resistance (Krokene et al., 1999) and the formation of traumatic resin ducts (Nagy et al., 2000). Franceschi et al. (1998, 2000) corroborated these conclusions by observations at the cellular level for the hypersensitive reaction and induced resistance in Norway spruce. Induced resin flow, by definition, is a wound response (Ruel et al., 1998); the presence of fungi could probably enhance it but no information is available yet to test this prediction. 3.1.2. Non specificity of tree responses This non-specificity results from the fact that tree responses are responses to wounding. I thus also hypothesize that all tree-induced reactions against bark beetles and their associated fungi are non-specific, which is that the corresponding qualitative changes in the tree tissues do not depend on the aggressors. Only the intensity of the changes varies with the nature of the aggressor. That has been demonstrated directly for different levels of tree reactions, through biochemical (terpenes and phenols) or histological approaches: hypersensitive reaction (Wong and Berryman, 1977; Delorme and Lieutier, 1990; Lieutier et al., 1991b; Brignolas et al., 1995a; Raffa and Smalley, 1995; Franceschi et al., 1998); wound periderm (Müllick, 1977); induced protection (Krokene et al., 1999); and traumatic resin ducts (Tomlin et al., 1998; Nagy et al., 2000). It is also a priori true for induced resin flow because it is typically a wound reaction. 3.1.3. Role of phloem parenchyma cells The phloem parenchyma cells play an essential role in the development of the hypersensitive reaction in regard to the syntheses of both terpenes and phenols. Previously suggested by Reid et al. (1967), Berryman (1972) and Lieutier and Berryman (1988a), Franceschi et al. (1998) recently demonstrated this role. Franceschi et al. (2000) subsequently generalized the role of the phloem parenchyma cells to all cases of tree response to bark beetles (except induced resin flow), although their influence on the formation of traumatic resin ducts (and the resulting induced protection) and wound periderm is indirect, as previously suggested by Bois and Lieutier (1999). The structure and development of the PP cells in Norway spruce have recently been presented in detail by Krekling et al. (2000).

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3.2. BIOCHEMICAL CHARACTERISTICS OF THE RESPONSE The products synthesized by the tree have been identified for the case of the hypersensitive reaction, but not for induced resin flow or traumatic resin ducts. Furthermore, studies have been conducted almost exclusively at the phloem level, where an increase of more than 100 times in terpene concentration was observed (Shrimpton, 1973; Raffa and Berryman, 1982b; Lieutier et al., 1991b; Raffa and Smalley, 1995), accompanied by an increase in the level of phenols and a reduction in free sugar concentration (Shrimpton, 1973). Although the relative composition of monoterpenes and resin acids varied slightly (Russell and Berryman, 1976; Raffa and Berryman, 1982b; Langström et al., 1992), the most important alteration was an absolute increase in the concentration of these substances (Delorme and Lieutier, 1990; Lieutier et al., 1991b; Raffa and Smalley, 1995). Phenols however show a considerable change in their relative composition, with the concentration of some compounds decreasing while others increase, some even being new for the tissue (Brignolas et al., 1995a; Lieutier et al. 1996a). However, no new compounds are synthesized at tree level, since the final composition of the phloem reaction zone resembles that of heartwood (Shrimpton, 1973; Lieutier et al., 1991a). Nonetheless, these compounds are new in the tissues where the reactions took place, at least for phenols. They originate from neosynthesis and not from a degradation of pre-existing products, since both an alteration of the enzymatic activity of the stilbene synthase (STS) and chalcone synthase (CHS) (Brignolas et al., 1995b), as well as gene activation (that is an increase of the mRNA of the enzymes STS and PMT [pinosylvine methyl transferase]), were observed (Chiron et al., 2000). For terpenes, the observed increase in terpene cyclases (Steele et al. 1995) and terpene synthases (Steele et al. 1998) results from a stimulation reaction, since the final products were previously present in the phloem. Although the synthetic pathways mentioned were studied in isolated reactions, they are correlated with tree resistance, as demonstrated by different authors, for the terpenes (Raffa et Berryman, 1982b; Christiansen, 1985b; among others) and the phenols (Shrimpton, 1973; Brignolas et al. 1995b, 1998; Bois and Lieutier, 1997). 3.3. ORIGIN OF THE ENERGETIC COMPOUNDS USED IN THE INDUCED RESPONSES Research in this field has tackled the hypersensitive reaction only. Since sugar and starch concentration in the phloem decrease rapidly in the close vicinity of the reaction zone (Shrimpton, 1973, Christiansen and Ericsson, 1986; Miller and Berryman, 1986), these compounds are certainly used by the tree as an energy source for the induced response. However, they may also be consumed by the fungus for its growth, at least inside the reaction zone. Also, the energy demand is considerable during the reaction process, especially when attacks are numerous, and most studies have concluded there is a mobilization of products from the current photosynthesis, at least at a high level of attack density (Christiansen and Ericsson, 1986; Miller and Berryman, 1986; Christiansen et al., 1987; Christiansen, 1992; Dunn and Lorio, 1992; Christiansen and Fjorne, 1993).

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3.4. MODE OF ACTION UPON THE AGGRESSORS The deterrence of the hypersensitive reaction upon the aggressive agents results from a combination of both physical and chemical effects, as well as from nutrient depletion in the reaction zone, which results in a reduced access to nutrients in the living tissues. Considering both types of aggressors, insects and fungi, the physical effects mainly consist in hardening of the resin impregnated tissues and resin flooding from the saturated tissues into the galleries; these have consequences on the beetles and fungi comparable to those of the preformed and induced resin flows. The chemical effects themselves result from complementary actions of several compounds from different chemical families rather than one particular group. In the following, I shall focus on the chemical effects. Reaction tissues and their resin are more toxic and repellent for beetles than control tissues and preformed resins, and they also inhibit fungal growth more efficiently (Bordasch and Berryman, 1977; Paine et al., 1987). This is certainly because a minimum concentration of defensive chemicals in the reaction zone appears to be crucial to contain the aggressors (Raffa and Berryman, 1983a; Christiansen et al., 1987). Assays with purified compounds point to which compounds are involved. At concentrations present in the reacting tissues, terpenes are toxic or repellent for beetles either by contact or vapor (Smith, 1963, 1965; Coyne and Lott, 1976; Bordasch and Berryman, 1977; Raffa and Berryman, 1983b, Raffa et al., 1985; Delorme and Lieutier, 1990; Raffa and Smalley, 1995). Contact and vapor have also inhibitory effects on the beetle-associated fungi (Cobb et al., 1968; Shrimpton and Whitney, 1968; Raffa et al., 1985; Bridges, 1987; Delorme and Lieutier, 1990). Raffa and Berryman (1987) claimed that, in general, terpenes showing the largest increases in the reacting tissues have the most deleterious effects on the beetles and their fungi. However, although some compounds such as limonene may be more toxic than others (Raffa et al., 1985), all monoterpenes exhibit a high toxicity for beetles and a high inhibitory effect for fungi at concentrations close to that in the reaction zones (Delorme and Lieutier, 1990). Effects of terpenes on both beetles and fungi thus seem to be due more to the total quantity of monoterpenes rather than to some particular compounds (Berryman and Ashraf, 1970; Raffa and Berryman, 1982a, b; Delorme and Lieutier, 1990; Lieutier et al., 1991b; Raffa and Smalley, 1995). Phenols have been assayed against fungi only and exhibited an effect by contact (Brignolas, 1995; Bois et al., 1999; Evensen et al., 2000). In opposition to terpenes, this effect is mainly due to particular compounds (Brignolas; 1995), and it is remarkable that these compounds are generally those which are neosynthesized in the reaction zone: pinosylvin and pinocembrin for pines (Hart and Shrimpton, 1979; Hart, 1981; Bois et Lieutier, 1997), stilbene aglycons for spruce, with some acting synergistically (Brignolas, 1995). However, the role of phenols is not clear yet and they have not been directly demonstrated to play a role in nature. Moreover, in vitro assays with wood pieces showed a very limited effect of phenols on various fungi and particularly species of Ophiostoma (Loman, 1970; Hart and Hillis, 1974; Hart and Shrimpton, 1979).

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4. ROLE OF THE DEFENSE SYSTEMS 4.1. RAPIDITY Rapid tree responses to attack by beetles and their associated fungi are critical in tree resistance, and the timing of the different sequences of the response is important. Under favourable climatic conditions, high populations of an aggressive bark beetle can completely terminate their aggregation in 4-5 days to one week and sometimes less (Payne, 1980; Raffa and Berryman, 1983a; Anderbrandt et al., 1988), whereas it can take two or three weeks when the climatic conditions are less favorable or for less aggressive bark beetles. Under these conditions, it is interesting to compare the delay of beetle aggregation with the rapidity at which the different resistance levels are built by the tree and at which the corresponding products can affect the aggressors. Even when the mechanisms of the response start very early, the essential delay for the tree is the appearance of sufficiently high concentrations of the secondary metabolites, since these are the final products that act on the aggressors. Preformed defenses need practically no delay to occur since they are present before the attack. High quantities of terpenes that are toxic for beetles (see references above) are liberated at the moment of wounding, but also decrease very rapidly. A reduction of the resin flow by 65% in 2-3 days has been reported for P. contorta subjected to high attack densities (Raffa and Berryman, 1983a). Resin flow can even dry up completely in 24 hours after wounding in loblolly pine (Ruel et al., 1998). Induced defenses, on the other hand, involve gene activation followed by important changes in cell metabolism or cell division patterns and differentiation, which takes time until the secondary metabolites appear at a high concentration. The quicker responses are those that involve the lowest changes. Induced resin flow needs three days to reach a high level (Ruel et al., 1998). This can allow it, however, to relieve the preformed resin flow. Then, the induced resin exuded from the sursaturated tissues involved in the hypersensitive response could, in turn, relieve the induced resin flow. Under these conditions, and if the three systems are effectively acting in the same tree, resin could potentially be emitted continuously by the tree. However, the existence of the induced resin flow has not been demonstrated yet in conifers other than loblolly pine. Resin impregnation of tissue due to the hypersensitive reaction is clearly visible in the phloem of pines, as soon as three days after fungus inoculation (Lieutier and Berryman, 1988a). Although maximum after three weeks, the extent of the reaction zone and the terpene content of the lesion are already very well developed in 10 to 15 days, while terpene concentration itself also reaches a maximum in 10 to 15 days (Raffa and Berryman, 1982b; Lieutier et al., 1990; Raffa and Smalley, 1995). However, the concentrations reached in the reaction zone, even if not maximum, rapidly become sufficient to be lethal for a majority of insects. In P. resinosa and P. banksiana, after three days, the concentrations reached in the phloem can kill 9095% of Ips pini (Raffa and Smalley, 1995). Regarding phenols, important modifications in the relative proportions are observed in less than 10 days, with some compounds increasing dramatically during that period (Brignolas at al.,

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1995a,b). Histological changes in the PP cells were considerable at 12 days (Franceschi et al., 1998). More complex changes are slower. The traumatic resin ducts need more than two weeks to be built locally, one year or more at a distance of several meters (Christiansen et al., 1999b, Nagy et al., 2000). Consequently, the very fast preformed response corresponds to the beginning of resistance, but it needs to be rapidly completed by other mechanisms for the tree to resist bark beetle attacks. Induced responses, especially induced resin flow when it occurs and the hypersensitive response, can certainly constitute a significant resistance to the aggressors, at least with terpenes, relaying and completing the effects of the preformed resin. The above considerations demonstrate that there is a remarkable complementarity and “cooperation” between the preformed and the different induced systems for at least two or three weeks following attack. However, the above reported changes associated with the development of the hypersensitive reaction have been observed after low-density inoculations. One may wonder, however, if the tree can produce the secondary metabolites so quickly in case of mass attacks (see below “beetle mechanisms of establishment”). Thus, the hypersensitive reaction may not be so efficient against outbreak populations, except when unfavorable climatic conditions occur for the beetles or when the resin flows (preformed and induced) slow the aggregation process significantly. Nevertheless, the most frequent situation is that of non-outbreak populations, which have difficulties reaching high densities rapidly. In such conditions, the hypersensitive reaction certainly plays a decisive role to protect the trees. The traumatic resin ducts probably interfere with the long-term resistance only. 4.2. RELATIVE ROLE OF THE PREFORMED AND INDUCED DEFENSES: A TREE STRATEGY? The mechanisms of the tree responses are increasingly elaborated and complex going from preformed to long term induced defenses. All defense systems are costly in terms of energy demand but they differ in the way the energy is used for defense. The advantage of the preformed system is that, since defenses are built before beetle attack, they are ready to act, with no delay, at the very moment beetles attack. However, a high quantity of energy has been mobilized, which can be of no use if no attack occurs. Alternatively, the advantage of induced defenses is to mobilize the energy for defense only if attacks occur and only at a quantity necessary to stop the aggressors. But this introduces a delay in the response of the tree, which is the longest for the most elaborate defense systems. On this energy basis, Matson and Hain (1985) have suggested that, in pines, preformed defenses would be predominant in situations (seasons, regions, tree species) where trees are subjected to heavy and repeated (continuous) attack pressure. Induced responses would be mainly used in situations where repeated attacks occur over multiple generations in a season. Indeed, preformed induced defenses have been observed to play an important role in loblolly pine and other southern pines which are subject to asynchronous attacks all year round, while the hypersensitive reaction plays the major role in lodgepole pine and other western and

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northern pines exposed to only a few beetle generations per year. Christiansen et al. (1987) have extended this hypothesis to all conifer genera, arguing that spruce and firs, which have non-efficient preformed defenses, live in cooler and more humid climates than pines where bark beetle attacks are less frequent. These theories presume that bark beetles have played a significant role in shaping the evolution of conifer defenses. The role of resin flow relative to the hypersensitive reaction seems however to depend essentially on the particular direction of the beetle maternal galleries (see below), in relation to the anatomy of the resin duct system. D. frontalis bores winding galleries, which sever numerous vertical resin ducts in loblolly pine. In beetles with vertical galleries such as D. ponderosae in the northern U.S. and I. typographus in Northern and Central Europe, few resin ducts are cut, while the hypersensitive reaction is stimulated because of its preferential development in the vertical direction. In Norway spruce, the hypersensitive reaction plays the main role in stopping the attacks of I. typographus (Christiansen and Horntvedt, 1983) while preformed defenses in the same trees are responsible for stopping attacks by D. micans (horizontal galleries) (Wainhouse et al., 1990; Lieutier et al., 1992). Pine Ips species can have more than two generations per year, especially in Southern Europe (Chararas, 1962), and although the hypersensitive reaction plays the most important role (Lieutier et al., 1988; 1995), they have vertical galleries. In southwestern China, Yunnan pine (P. yunnanensis) is attacked simultaneously by T. piniperda (vertical galleries) and T. minor (horizontal galleries) (Ye and Ding, 1999). In firs, which have no resin duct system, of course only induced defenses interfere regardless of the orientation of the galleries, as for S. ventralis and its horizontal galleries. In fact, it seems that all kinds of galleries and beetle behaviors can be found in all tree species. Closer to the theory proposed by Raffa and Berryman (1987), it thus seems more reasonable to consider that the beetle species have adapted (in various ways) their behavior and attack strategy to the existing host mechanisms of resistance than to consider that tree defense strategies have evolved in response to the attack behaviour of few beetle species. Submitted to attacks by various xylophagous insects, conifers have probably elaborated a wide array of defense mechanisms, all present in the different conifer species to varying degrees, to try and contain all kinds of attacks (this may be the reason why all tree responses are basically not specific as to the aggressors). Then, beetle strategies have evolved to try and cope with the host defense mechanisms, but differ according to beetle species, each of them evolving its own attack strategy, even in the same conifer species (See below beetle strategies). This does not preclude, however, the possibility that some particular tree compounds may have evolved under the effect of bark beetle attacks (Sturgeon and Mitton, 1982). Lombardero et al. (2001) have suggested that environmental factors could have different effects on the constitutive and induced defenses (resin flows) in loblolly pine. The predominance of one or the other defense system in the same tree could thus depend on environmental conditions. If it were verified for the hypersensitive reaction also, this suggestion would corroborate the above hypothesis, since it could explain the particular (sinuous) pattern of D. frontalis galleries.

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Otherwise, an interaction between the different defense systems is certainly frequent. That has been mentioned above (see II.1.1.) between the constitutive defense and the hypersensitive reaction of spruce against D. micans (Wainhouse et al., 1997). In P. contorta, the rate of preformed resin flow conditions the emission of aggregation pheromones by the pioneer D. ponderosae (Raffa and Berryman, 1982a). Since a rapid aggregation is necessary to overcome the tree’s induced defenses (see VI.1.1.), this underlines again interactions between preformed and induced defenses (Raffa et al., 1993). Moreover, at least for phenols, the same PP cells seem to be involved in constitutive, hypersensitive and delayed resistance (Franceschi et al., 2000), which means an interaction among these different systems. 5. BEETLE MECHANISMS OF ATTACK AND ESTABLISHMENT With such sophisticated and elaborate defense systems complementing each other in the tree, how can bark beetle attacks succeed? This point will be discussed while referring to the most frequent situation: exhaustion of tree defenses associated with beetle establishment and tree death, which corresponds to the situation of most tree killing bark beetle species. Paine et al. (1997) stated that it is critical, at this step, to distinguish between exhaustion of tree defenses and sapwood occlusion and colonization by fungus. More broadly, this can be extended to phloem colonization by beetles. However, as we shall see below, it does not seem that this distinction can really, be done in time, since phloem and sapwood invasions start before defenses are exhausted. 5.1. EXHAUSTION OF HOST DEFENSES Considering the hypersensitive reaction, Shrimpton (1978) suggested that the fungi introduced by the beetles at the moment of attack kill the tree cells, leading to no more resin synthesis and secretion, thus allowing the establishment of the beetle population. Tree death would thus be a pre-requisite to the invasion by the aggressors. In fact, the stopping of resin production would not be caused by cell death, but rather by an exhaustion of the ability of the tree to synthesize resin. The problem would thus stand at the level of the tree itself and not at the level of the defense reaction. 5.1.1. The mechanisms Rapidity, together with a minimum number of simultaneous attacks, is necessary for beetle success. Various observations demonstrate that a threshold of attack density (number of attacks per unit bark surface) exists above which the attacks succeed, while they fail below (Berryman, 1976, 1982; Raffa and Berryman, 1983a; Christiansen et al., 1987). The existence of such a threshold is explained by the necessity of weakening tree resistance. According to Hodges et al. (1985) and Nebeker et al. (1993), in the southern US, a number of attacks would be necessary to ensure a complete circumferential introduction of fungus into the tree, a necessary condition for the fungus to produce toxins that would alter physiological processes

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in the tree, weaken its resistance and make it more susceptible to subsequent attacks. Another explanation, proposed for situations in the northern US and Europe, is based on energetic considerations. Indeed, syntheses of the secondary metabolites (terpenes and phenols) involved in resistance are energy-demanding processes (Croteau et al., 1972; Croteau and Loomis, 1975). Their stimulation by numerous attack points in rapidly increasing numbers would increase the energy demand considerably. Above a certain density of attacks (threshold of attack density), the tree would not have any more capacity to rapidly mobilize the energy necessary to keep the induced or stimulated metabolic activities at a high level in all zones of attack. The concentrations of defensive chemicals in the reaction zones would thus not increase rapidly enough or to a sufficient level to contain the aggressors, and attacks would succeed. If the beetle attack density stays below this critical threshold, tree defenses would not be depleted and attacks would finally fail. The existence of a threshold of attack density has been demonstrated in various tree species after natural beetle attacks (Waring and Pitman, 1980, 1983; Mulock and Christiansen, 1986; Langström et al., 1992; Langström and Hellqvist, 1993; Guérard et al., 2000). According to that strategy, the role of a high number of attacks is to induce numerous reactions that will be stimulated by the beetles tunneling activity and the presence of fungi. The role of fungi in accelerating tree energetic expenditures and thus lowering the threshold is evidenced by observations of natural infestations with little or no blue stain, in which attack densities were higher than in situations where blue stain fungi were present (Whitney and Cobb, 1972; Bridges et al., 1985). Similarly, and simulating bark beetle attacks, it is possible to experimentally define a critical threshold of inoculation density (for a given height of inoculation belt) above which tree resistance is overcome and the tree is killed (Raffa and Berryman, 1983b; Horntvedt et al., 1983; Christiansen, 1985b; Langström et al., 1993; Solheim et al., 1993; Croisé et al., 1998a; Guérard et al., 2000). However, this threshold is weakly related to the critical threshold of attack density (see the reasons in VI.3). It is important to remember that, while boring their galleries into the phloem, beetles most often damage the cambium and the surface of the sapwood as well, and consequently inoculate the tree with the fungi at these different levels. Artificial fungus inoculations do the same since they are performed at the cambium level. Tree resistance and the development of hypersensitive reactions thus take place simultaneously in each of these tissues from the very beginning of the attack, against the beetle and fungi in the phloem and cambium, and against the fungi in the sapwood. The mechanisms described above of exhaustion of tree defense thus take place in all these tissues, especially in the phloem and the sapwood because of their larger volume. 5.1.2. The rapidity of the stimulation In Norway spruce, artificial inoculations with a fungus (O. polonicum) have been reported to begin to stimulate the quantity of secondary metabolites induced by wounding after only 7 or 10 days (Brignolas et al., 1995a). This may seem too slow for that stimulation to rapidly lower the threshold of attack density and allow beetle establishment. However, the important thing in the above strategy is not the final

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products but rather the mobilization of the energetic resources. The mechanisms of the hypersensitive reaction start largely before seven days as does the mobilization of the energetic resources. Regarding phenols, stilbene synthase and chalcone synthase activities in Norway spruce are already very strongly stimulated six days after inoculation (Brignolas et al., 1995b), demonstrating that the stimulation starts largely before day six. In Scots pine, after wounding, the mRNA of STS and PMT have already increased considerably in three days, indicating that the tree response started before three days after the attack, although no earlier measurements occurred. After a fungus inoculation, a higher increase occurs with the same delay, thus demonstrating early stimulation (Chiron et al., 2000). Considering terpenes, monoterpene synthase activity in the hypersensitive reaction zone has already increased three fold six hours after wounding and ten fold in two days, with the maximum being reached in 12 days (Steele et al., 1998). Diterpene and sesquiterpene synthase activities increase a few days later but this is not surprising since monoterpenes act as a solvent for these more complex compounds. It is very likely that equally rapid responses in enzyme activities exist for the induced resin flow too. 5.1.3. Conditions for fungus efficiency By themselves, the fungi do not stimulate the tree defense mechanisms under any circumstances. In the phloem hypersensitive response in particular, a minimum number of spores must be introduced into the tree by the beetle. Indeed, the existence of a positive relationship between the number of spores artificially introduced and the concentration of secondary metabolites in the phloem reaction zone has been demonstrated (Lieutier et al., 1988, 1989a). In most experiments with trees, artificial inoculations with 5 mm diameter discs of agar cultures are used to study the tree response and to understand the role of the fungus in the tree-bark beetle relationships. Such discs, however, contain such a high number of spores (for example, more than one million in a 5 mm diameter disc of a 3-week old culture of Leptographium wingfieldii, a fungus associated with T. piniperda) that the tree reaction is always stimulated and maximum (Lieutier et al., 1989a). Certainly, the beetles do not carry such high numbers of spores. Interpretations and conclusions regarding the role of the fungi during beetle attacks must be taken with care when they are made based on experiments using artificial inoculations, because they may not correspond to the natural situation where the fungus is introduced into the tree by the beetle itself. 5.2. TISSUES COLONIZATION AND TREE DEATH It is very difficult to define the moment of tree death. Paine et al. (1997) considered that “gallery construction and oviposition can be used as a bioassay to indicate when tree mortality has occurred”. However, tree death is very likely a continuum of events beginning with exhaustion of tree defenses (just before oviposition) and finishing with the blockage of sapwood water transfer and the fading of foliage (which can take place several weeks after beetle oviposition).

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According to Paine et al. (1997), the assumption that fungi play an important role in killing trees attacked by bark beetles is based on the following observations: most bark beetles vector staining fungi; the sapwood of bark beetle killed trees is stained; and trees can be killed by artificially mass inoculating them with the fungi. Many papers have been published in these directions and references can be found in the review by Paine et al (1997). We can also add that beetles which do not vector fungi, either succeed in establishing in their host without killing it (D. micans or Dendroctonus punctatus for example), or are very secondary beetles which only attack trees that are already dead. Nevertheless, all these observations do not allow definitive conclusions about the role of fungi in the tree killing process. They even do not allow concluding that fungi are involved in tree death at all. Indeed, there is still the possibility that fungi exploit the beetle for transportation and invade the sapwood after the tree has been killed by something else. Artificial mass inoculations may not represent the situation of natural attacks (see below the case of T. piniperda). Also, the lack of fungi associated with D. micans may be the consequence of the beetle not killing its host and not the opposite. Moreover, trees have been reported to be successfully colonized and killed by bark beetles without blue stain fungi (Ophiostoma) (Whitney and Cobb, 1972; Bridges et al., 1985). On the other hand, Pinus taeda attacked by Dendroctonus frontalis have been observed to remain alive despite extensive blue stain in the sapwood (Nebeker et al., 1993). It is possible, however, that fungi other than blue staining ones play a role. However, there must be a reason why most tree killing bark beetles are associated with blue stain fungi. Stimulating tree defenses and helping in overcoming tree resistance is certainly a good and sufficient one. In fact, beetles do not need fungi to kill the tree but only to exhaust tree defenses. After host defenses are exhausted, beetle establishment can begin. But, at this moment, since pathogenic fungi are present in the tree, they certainly play a role in the subsequent tree killing process, although it is probably not their primary role. Another important fact to consider is that, although variations in pathogenicity exist among species of fungus, all bark beetle associated blue stain fungi are only moderately pathogenic. Tree death very likely results from several phenomena acting in concert. Berryman (1972) already suggested that a tree is killed as a result of simultaneous actions of the insect and fungus rather than successive action of vector and pathogen. Beetles and fungi already cooperate in overcoming tree resistance and their respective role in that step has been presented above (see also below), but little is known regarding their respective roles in tree death. When tree resistance has been overcome, beetle establishment begins and death of the tree is considered as assured (Berryman, 1982; Wood, 1982). As already mentioned, exhausting tree resistance can be completed in few days. However, tree death comes much later with disruption of water transportation, sapwood occlusion and fading of the foliage (DeAngelis et al., 1986; Nebeker et al., 1993; Lorio et al., 1995). Sapwood invasion by fungi probably plays a role in tree death, but the mechanisms are certainly more complex than this alone. Fourteen days after attack by D. ponderosae, lodgepole pine sapwood is occluded to a depth of only 20 mm (Solheim, 1995), and the fungus invades not more than 18 % of the tracheids until

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10 weeks have passed (Ballard et al., 1984). Likewise, in Norway spruce fungi are present in the sapwood at a depth of 18 mm five weeks after successful attacks by I. typographus (Solheim, 1992). Several other similar observations are reported in the review by Paine et al. (1997). One may thus wonder if tree resistance has really been completely exhausted at this time in the sapwood, or if fungi are really involved in tree death. Perhaps fungi can kill trees with toxins (DeAngelis et al., 1986; Hodges et al., 1989). Moreover, the presence of a certain area of blue stained sapwood in trees resisting beetle mass attacks or artificial mass inoculations with fungi demonstrates that colonization of tree tissues starts during the process of defense exhaustion. This phenomenon has even been frequently cited to account for comparisons of the resistance levels of different tree categories (Christiansen and Berryman, 1995; Christiansen and Glosli, 1996; Bois and Lieutier, 1997; Brignolas et al., 1998; Krokene et al., 1999, among others). In addition, in response to increasing densities of fungus inoculations staying below the critical threshold, sapwood occlusion gradually increases along with the quantity of non-functional sapwood (Guérard et al., 2000). Mechanisms other than fungus invasion also obviously interfere. The beetle population itself while colonizing the phloem, and consequences of other events taking place in this tissue, certainly play a role at this stage, since tree death is more rapid after insect attacks than after artificial mass inoculations. Moreover,

the relations between foliage symptoms, sapwood drying and occlusion, and fungus extension into the sapwood are not clear (Parmeter et al., 1992; Harrington, 1993; Hobson et al., 1994). As in the exhaustion of tree defenses, tree death certainly results from a combination of effects from bark beetles and the fungi they vector. In

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addition, sapwood tree defense mechanisms themselves may also contribute significantly in sapwood occlusion and tree death when defense reactions lead to extended resin soaking in the sapwood. Indeed, following artificially induced mass attacks by T. piniperda on Scots pines baited with terpenes, some of the killed trees had about 30% of their sapwood section soaked with resin with no blue stain; the resin impregnated zones were located exactly beneath the galleries (Figure 8 and Lieutier et al., unpublished). 5.3. CONCLUSIONS It is not at all obvious that the death of the tree is a prerequisite for beetle establishment. Rather, it seems that beetle population establishment proceeds in two successive (and not simultaneous) steps: 1- exhaustion of tree defense; 2- tree killing and completion of invasion of the tree tissues by the aggressors. This statement is in agreement with the conclusions by Parmeter et al. (1992), Nebeker et al. (1993) and Hobson et al. (1994). Meanwhile, Berryman’s statement about tree killing (1972) can be enlarged and specified by inferring that both insect and fungi are needed to kill the tree after both are needed to overcome its resistance. The phenomena involved during the time sequences leading to beetle establishment would be the following: First, tree resistance is weakened, through the stimulation of tree defense mechanisms leading to their exhaustion by the aggressors. During that first step, the aggressors begin to invade the tree tissues (beetles and fungi in the phloem, fungi in the sapwood), but their extent remains very limited by the still efficient defenses of these tissues. Next, after the tree defenses are exhausted, the aggressors freely invade non-resistant tree tissues, while the tree dies as a result of exhaustion of its defenses. The free invasion of the tree tissues has two components: 1- rapid invasion of the phloem by the insects, with oviposition and brood development, i.e., beetle population establishment; 2- slow invasion of the sapwood by the fungus, associated with sapwood occlusion. The establishment of the beetle population thus begins before the tree is killed, as soon as the tree’s resistance is overcome. One may wonder why the tree killing bark beetles are not associated with highly pathogenic fungi. Indeed, such fungi would exhaust tree defenses and kill the tree with just a few inoculation points, whereas moderately pathogenic fungi need many inoculation points for the same results. The reason could be the necessary existence of the above two steps for successful brood development. Indeed, if a highly pathogenic blue stain fungus exhausted a tree’s defenses and killed the tree very rapidly, it would also certainly invade the whole tree very rapidly before the beetle and its brood became established, making the host tissues unsuitable for brood development. An association with a moderately pathogenic fungus is a better strategy for the beetle. It allows beetles to overcome tree resistance while limiting fungus extension, thus preserving the quality of the substrate for the beetle’s progeny. Protecting the quality of the tree’s tissues may also be a reason for not killing the tree before beetle establishment begins. The existence of the two successive steps presented above is thus a necessity for the brood to find a suitable substrate, as well as the logical consequence of an association with only moderately pathogenic fungi.

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6. BEETLE COLONIZATION STRATEGIES Raffa (1991) proposed three kinds of colonization strategies for bark beetles attacking living trees: overwhelming the defenses of healthy trees; avoiding resistant trees; and avoiding/tolerating resistant responses within trees. According to Raffa et al. (1993), the first situation corresponds to an aggressive strategy developed by the regular tree killers (near-obligate parasites), while the second one corresponds to a non-aggressive strategy developed by saprophytic (facultatively parasitic) species. However, since the resistance of living trees is never nul, beetles belonging to the second group, when arriving on their host tree, necessarily still have to choose between overwhelming tree resistance and avoiding tree responses. If they were able to avoid tree responses, very likely they would be able to develop in healthy trees. Consequently, they certainly use the strategy of overwhelming tree resistance. Closer to what has been suggested by Lieutier (1992), I thus propose to distinguish two basic colonization strategies for all bark beetle species attacking living trees: 1Exhausting tree defenses and killing the tree, corresponding to the above presentation. In that strategy, two sub-groups can be distinguished according to host vigor (healthy versus weakened). 2- Avoiding / tolerating tree defenses and keeping the tree alive. 6.1. EXHAUSTION OF TREE DEFENSES: THE COOPERATIVE STRATEGY Overcoming tree resistance is the first task that the beetles must perform. It is accomplished through exploiting tree defense mechanisms by stimulating the induced responses. This can be done in various ways but a high number of simultaneous attacks are always necessary, leading me to call this strategy the “population strategy” or the “cooperative strategy”. The tree is then killed as an unavoidable consequence of defense exhaustion, especially through invasion of its tissues by the aggressors: fungi in the sapwood, and beetles in the phloem. This strategy can thus also be compared to that of a parasitoid. Most bark beetle species attacking living trees belong to that category, be they primary or secondary species. Only the way used to exhaust tree defenses and to overcome its’ resistance differs. Examples of variations on such a strategy are presented below. 6.1.1. The “typical / classical” situation This corresponds to the above-described mechanisms. A quick aggregation is necessary to rapidly weaken the tree and not allow it enough time to develop an extended local hypersensitive reaction or to build traumatic resin ducts. Aggregation pheromones are thus a very useful tool for species using that strategy (Wood, 1982; Raffa and Berryman, 1983a). As long as the critical threshold of attack density is not reached, the beetles that have already arrived continue to release aggregation pheromones. If too low a number of beetles rapidly aggregate on the tree, the attack density stays below the threshold, tree defenses cannot be exhausted and the attack finally fails. On the contrary, if a sufficiently high number of arrivals allow the beetle population to rapidly reach the critical threshold, tree resistance is

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overcome. The pheromone emission is then stopped which limits further intraspecific competition among the brood members (larvae and callow adults) (Berryman, 1982; Raffa and Berryman, 1983a; Birgersson and Bergström, 1989; Raffa et al., 1993). During the aggregation process, all contributions to deplete the tree’s ability to synthesize secondary metabolites and thus to exhaust the tree’s defenses are important in order to overcome the tree’s resistance. , Anything that lowers the critical threshold helps to improve the probability that the attack will be successful. In this context, the pathogenic fungi introduced by the beetles play an essential role through stimulating tree syntheses (Berryman, 1976; Whitney, 1982; Raffa and Berryman, 1983a; Christiansen et al., 1987; Lieutier, 1992; among others). Similarly, attacks during the season of active tree growth and vertical beetle galleries fit in with this strategy because they stimulate the tree’s metabolic activity (Lieutier, 1992). As a summary, the “classical” situation in the strategy of exhausting tree defenses is that of bark beetle species typically filling and sharing the following four main conditions: ability to release aggregation pheromones; association with phytopathogenic fungi; attack during the season of maximum tree activity; and vertical egg galleries. On the other hand, tolerance to resin can change with beetle species, depending on the vigor of the trees that are usually attacked. That strategy concerns I. typographus, D. ponderosae, D. brevicomis, I. acuminatus, etc., and most other bark beetle species that synthesize aggregation pheromones and attack Pinus, Picea or Larix. Although using the same general strategy, all these species can be ranked along a vigor gradient defined by the quality of the hosts that they can attack, from the real tree killers that attack healthy trees to the species attacking very weakened trees. It is also a ranking of beetle efficiency in overcoming tree resistance. Because they have developed the most efficient mechanisms for that task, the tree killing species have access to a large quantity of food that is not available for the other ones. This has led to considering them as the most evolved species (Raffa et al., 1993). 6.1.2. Other closely related situations There are situations where the above 4 conditions are not all filled, although the same strategy is used. T. piniperda has no aggregation pheromone but aggregation occurs due to the attractiveness of monoterpenes emitted through the wounds caused by the pioneer beetles (Byers et al., 1985; Schroeder, 1987). This beetle is associated with a fungus of the genus Leptographium everywhere this association has been looked for: L. wingfieldii in Europe (Lieutier et al., 1989b; Gibbs and Inman, 1991; Solheim and Langström, 1991), Leptographium yunnanensis in southern China (Zhou et al., 2000). However, the beetles themselves, without the help of a fungus, overcome tree resistance. Indeed, the associated pathogenic fungus L. wingfieldii is unable to stimulate the hypersensitive reaction when it is introduced into the host tree by the beetle itself (Lieutier et al., 1989a, 1995; Lieutier, 1995), although artificial inoculations lead to violent reactions and its’ pathogenicity is high (Lieutier et al., 1989b; Solheim et al., 1993; Croisé et al., 1998a). This discrepancy has been attributed to the low number of spores introduced into the tree by the beetle (Lieutier

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et al., 1989a, Lieutier, 1995). Moreover, the percentage of beetles carrying the fungus is very low, around 5% (Lieutier et al., 1989b; Solheim et Langström, 1991). Thus, during attacks by T. piniperda, only the repeated mechanical wounds caused by the tunnelling insects can stimulate the tree’s hypersensitive reactions, which lead to exhaustion of the tree’s defenses (Lieutier, 1993; Lieutier et al., 1995). Under these conditions, overcoming tree resistance is difficult. Lieutier (1995) suggested that it is the reason why T. piniperda can only establish successfully on very weak trees in Europe. In such a situation it is also certainly easier to exhaust the host’s defenses when tree metabolism is low. Attacks by T. piniperda always take place largely before the trees start their activity in spring. After tree resistance is overcome and certainly also because the fungus pathogenicity is rather high, L. wingfieldii can invade the sapwood, even if the number of inoculation points is low. The situation with T. piniperda is a clear example that intense hypersensitive reactions (after low density artificial inoculations) and high pathogenicity (measured through mass artificial inoculations) are not proof that the fungus plays a role in stimulating the defense reactions, and thus in exhausting tree defense during natural attacks (see above V.1). D. frontalis follows the same general strategy in P. taeda, but it bores winding galleries. P. taeda is the species where the existence of the induced resin flow has been reported. The particular boring behavior of D. frontalis leads the beetles to cut numerous resin ducts while boring the horizontal part of the galleries, which probably explains why resin flows (constitutive and induced) play an important role in tree resistance (Nebeker et al., 1993; Paine et al., 1997; Ruel et al., 1998). But the hypersensitive reaction also plays a role (Paine and Stephen, 1988) because it is actively stimulated while the beetles bore the vertical and oblique parts of their galleries. Tree defenses are thus probably exhausted through stimulation of both the induced resin flow and the hypersensitive reaction. In addition, D. frontalis has aggregation pheromones and it attacks trees during their period of physiological activity. Fungi also certainly play a role in helping the beetle in overcoming tree resistance. However, in some situations and as for T. piniperda, death can occur without sapwood invasion by blue stain fungi (Bridges et al., 1985). S. ventralis bores transversal galleries in Abies. This behavior is not a handicap since there are no resin ducts containing preformed resin in firs. Only resin pockets (blisters) are disseminated in the cortex of the bark and thus are not met after the phloem has been reached. Moreover, the beetles seem to be able to avoid them (Ferrell, 1983). It is not known if aggregation pheromones exist but aggregation occurs and a symbiotic fungus is present which stimulates the hypersensitive reaction and then kills the tree by invading the sapwood after exhaustion of tree defenses (Berryman and Ferrell, 1988). Artificial mass inoculations with fungi are probably relevant to the same strategy when they lead to tree death. At first, tree resistance is overcome through wounding followed by stimulation of the hypersensitive reaction by fungi. Invasion of the sapwood and the phloem by the fungi may be thought to occur after tree defenses are exhausted. This is why the fungus model can be valuable for studying many aspects of the conifer - bark beetle relationships.

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6.2. AVOIDING / TOLERATING TREE DEFENSES: THE SOLITARY STRATEGY These beetles do not exploit the tree’s defenses to overcome the resistance of their host, but they avoid or tolerate them. Typically, everything is done to minimize the development of tree defenses. Only the local particularities of the stem or branches of the host, at the place of each beetle attack, determine the success or the failure of the attacks. Since there is no need for exhausting tree defenses, no cooperation is necessary and the beetles behave individually, leading me to call this strategy the “individual strategy” or the “solitary strategy”. As a logical consequence, the whole beetle life cycle can take place without killing the tree, making that strategy comparable to that of a parasite. Very few primary bark beetle species attacking living trees are representative of this situation. Examples are given below. 6.2.1. The typical situation Dendroctonus micans in Norway spruce in Europe is a good example. The hypersensitive reaction is minimized by boring transversal female galleries and by the absence of associated pathogenic fungi (Lieutier et al., 1992). Because of its transversal gallery, the boring female must face the preformed resin flow but this flow is weaker in spruce than in pines and the adults of D. micans are highly resistant to resin (Grégoire, 1988). Aggregation pheromones do not exist at the adult stage corresponding to an individual attack behavior. Local particularities of the bole (preformed defenses) determine if the female can lay eggs. They include preformed resin flow (Lieutier et al., 1992), stone cell masses (Wainhouse et al., 1990, 1998), and moisture and stilbene content (Storer and Speight, 1996). Eggs and larvae, which are directly facing the hypersensitive reaction since larvae are boring vertically, are also very tolerant to resin (Everaerts et al., 1988). Broods develop without killing the tree and several beetle generations can follow each other in the same tree before tree death occurs (Vouland, 1991). Opposite to the previous strategy, the “classical” situation in the strategy of avoiding or tolerating tree defenses is bark beetle species that meet the following four main conditions: no aggregation pheromones at the adult stage; no association with a phytopathogenic fungus; horizontal galleries; and a high tolerance to resin for both the adult and the larval stages. On the other hand, the period of attacks can be anytime in the year since defenses are avoided. D. punctatus in North America corresponds to the same situation as D. micans in Europe. Because the trees stay alive while undergoing successful attacks for several years, the question is raised regarding the role of the traumatic resin ducts. Numerous resin ducts are built around the zone of brood development. Moreover, a tree already attacked by D. micans is more easily attacked the following years with the new attacks localized preferably in close vicinity to the previous ones, which is at the place where the traumatic resin ducts are the most developed. The effective role of these ducts is thus questionable and one may wonder if they interfere with beetle establishment and tree resistance. Beetles are very tolerant to resin and it is also possible that, by obliging the tree to build resin ducts continuously year after

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year, they weaken it until it dies. Nothing is known about the cause of the death in a tree attacked by D. micans. 6.2.2. Other closely related situations D. valens and D. terebrans have a biology very similar to that of D. micans and D. punctatus and they probably use the same strategy. They have no aggregation pheromone at the adult stage, do not mass attack their host trees, and can reproduce in living trees without killing them (Raffa, 1991). Their eggs are also very tolerant to resin. They differ from D. micans in that they are associated with a highly pathogenic fungus (L. terebrantis) which causes extensive defense reactions when artificially inoculated to the host at a low density (Barras and Perry, 1971, Raffa and Smalley, 1988). However, it has not been demonstrated that this fungus causes the same hypersensitive reaction when introduced into the tree by a beetle, and it has also not been shown that it plays a role in exhausting tree defenses and in promoting beetle establishment. Likewise, no advantage has been revealed for the beetles from harbouring the fungus . As for D. micans, the beetles’ strategy thus seems to be an individual one of avoiding and tolerating tree defenses. The presence of the fungus is probably just a passive vectoring of a disease. 6.3. BEETLE AGGRESSIVENESS AND FUNGUS PATHOGENICITY The description of the cooperative versus solitary strategies above raises issues regarding beetle aggressiveness. In the solitary strategy, the ability of the beetles to develop in live trees makes them all aggressive (primary) species. In the cooperative strategy, the efficacy of the fungus in stimulating the reactions and exhausting tree defenses is essential for successful beetle attack. There is no relationship between beetle aggressiveness (primary versus secondary beetles) and fungus pathogenicity (Harrington, 1993; Paine et al., 1997). Pathogenicity is the ability of the fungus to kill the tree. It is measured by artificial mass inoculations in the case of beetle-associated fungi and it thus differs from the ability of the fungus to stimulate tree defenses during a natural beetle attack (see comments above). O. polonicum is associated with I. typographus, a very aggressive bark beetle, O. ips and O. brunneo-ciliatum are associated with I. sexdentatus and I. acuminatus, two moderately aggressive beetles, and L. wingfieldii is associated with T. piniperda which is characterized by a very low aggressiveness (it is sometimes considered as a secondary beetle). However, O. polonicum and L. wingfieldii are both highly pathogenic fungi, as shown by artificial mass inoculations to the host trees (Horntvedt et al., 1983; Christiansen, 1985b; Solheim and Langström, 1991; Solheim et al., 1993; Croise et al., 1998a). Also, both of them strongly stimulate tree defenses when artificially inoculated into the beetle’s host tree at low densities (Christiansen and Horntvedt, 1983; Lieutier et al., 1989b). O. ips and O. brunneociliatum have a very low pathogenicity (Guerard et al., 2000) and moderately stimulate host tree reactions (Lieutier et al. 1989b) when artificially inoculated. Thus, when fungi are artificially inoculated to trees, there is no relation between beetle aggressiveness and fungus pathogenicity. There is also no relation, in this

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artificial situation, between beetle aggressiveness and the ability of the fungus to stimulate the tree’s defenses. However, the results of research on the relationships between I. typographus, O. polonicum and Norway spruce have demonstrated that O. polonicum has a high ability to stimulate the tree’s reactions in cases of natural attacks by beetles and thus the fungus helps greatly in exhausting tree defenses (Christiansen et al., 1987). Studies on the relations between I. sexdentatus, O. brunneo-ciliatum (or O. ips) and Scots pine have demonstrated that O. brunneo-ciliatum has a moderate ability to stimulate the tree’s reactions (Lieutier et al., 1995). Opposite to O. polonicum and in spite of its similar high pathogenicity, L. wingfieldii is absolutely unable to stimulate the hypersensitive reactions of the host in cases of natural attacks by T. piniperda (see above). Thus, it seems that there is a relation between beetle aggressiveness and the ability of the fungus to stimulate the tree’s reaction during a beetle attack. We can thus hypothesize that, for beetle species choosing the cooperative (exhaustion) strategy, beetle aggressiveness is directly related to the ability of the fungus to stimulate the tree’s reaction during a beetle attack. The ability to kill the tree after exhausting its’ defenses may be related to fungus pathogenicity, but this is nota requirement. Instead, it may be related to the ability of the fungus to grow into the sapwood. The percentage of contaminated beetles does not need to be very high for that step (as in the case of T. piniperda). From the above discussion, I conclude that there is no relation between fungus pathogenicity (measured by artificial inoculations) and the ability of the same fungus to stimulate the tree’s hypersensitive reaction during a beetle attack. Consequently, there are certainly only very weak relations, if any, between the threshold of attack density and the threshold of inoculation density. This is in part due to the fact that frequently much less than 100% of the beetle population carries the fungus, and that the number of fungus spores introduced by a beetle into a tree certainly differs greatly from that contained in an artificial inoculation (see VII.2). However, determining the critical threshold of inoculation density can be very useful to compare the resistance level of different tree categories or to compare fungus pathogenicity. 7. QUESTIONS AND RESEARCH PROSPECTS Several aspects of the conifer – bark beetle – fungus relationships related to tree resistance are still not understood and need to be investigated. 7.1. DEFENSE MECHANISMS In addition to specifying the mechanisms and the effects of the newly discovered defenses (especially “preformed induced resin” and “induced resistance”), several aspects of the “old” mechanisms still remain to be understood. The defense mechanisms have almost always been studied with low-density inoculations, when the tree easily stops the aggressors, but several questions need to be answered to understand how tree resistance is overcome. How do the defense mechanisms work

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when the attacks are close to the critical threshold of attack density? Do they work in the same way as when inoculation (i.e., attack) densities are low? What critical changes occur in defense mechanisms when the threshold is reached? Are the changes qualitative or quantitative? Are the reactions suddenly inefficient or does their efficacy decrease gradually? Is the crossing of the threshold brutal or progressive -- do all attacks fail below the threshold and all attacks succeed above, or is there a progressive increase in the percentage of successful attacks? The hypersensitive reaction has been mostly studied in the phloem but the existence of resin-impregnated zones in the sapwood demonstrates that resistance takes place at this level also. However, sapwood defense mechanisms have almost never been investigated in the case of bark beetle attacks. Paine et al. (1997) stated that exhausting the host defense system corresponds to phloem colonization, but the development of sapwood defenses also certainly contributes to exhausting the host’s defenses. 7.2. STIMULATION OF THE INDUCED REACTIONS The importance of wounding in the elicitation and development of all kinds of tree defenses emphasizes the role of the insect itself and its boring activity. This role has been largely under-estimated until now and should be investigated thoroughly. The respective role of the beetle and the fungus in the stimulation of tree defense reactions must be clarified, as well as the way the fungus stimulates the defense mechanisms (additional wounds, enzymes). In addition, the real demonstration of this role for the fungus should be looked for in several tree - bark beetle - fungus relationships. Indeed, the presence of a pathogenic fungus carried by the beetle is not sufficient proof by itself (cf. T.piniperda ). The percentage of beetles contaminated by a fungus varies greatly among beetle species, and even for the same fungus and beetle species among different localities and years (Paine et al., 1997). It is usually very low for I. typographus (Solheim, 1993; 1995; Viiri and von Weissenberg, 1995) and Ips cembrae (Redfern et al., 1987), but it reaches almost 100% for I. sexdentatus and I. acuminatus (Lieutier et al., 1989b; 1991c). The meaning of the percentage of beetles contaminated by a given fungus species is thus questionable. If the fungus is needed to exhaust tree defenses, why is the percentage of association not always 100%, and what is the exact role of the fungus in stimulating the tree’s reactions if the percentage of association varies? If we consider the strategy of exhausting tree defenses, the answer may relate to variations in the ability of the fungus to stimulate the tree’s reaction. For the same beetle species, the role of the fungus may also depend on beetle population levels (see below VII.7.). In addition, the composition of the fungus flora associated with a given beetle species varies considerably among localities (Harding, 1989; Solheim, 1993), raising questions similar to those presented for the percentage of contamination. Related questions refer to the mechanisms involved in these variations. There are several questionable aspects regarding the relations between the thresholds of inoculum density and of attack density. It has been suggested above

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(VI.3) that they are not related. An important question relates to the observation that these two thresholds are frequently very close to each other, even when the percentage of association between the fungus and the beetle is very low [see Langström et al. (1992) compared with Solheim et al. (1993), Christiansen (1985b) compared with Mullock and Christiansen (1986), Raffa and Berryman (1983a), Lieutier (1995), Guérard et al. (2000) among others)]. In the later case, we would expect a much higher value for the threshold of beetle attack density. A similar value for the two thresholds thus means there is no fungal role in stimulation of tree defenses during natural attacks. What are the implications of this? The answer could greatly help in our understanding of the tree - bark beetle - fungus relationships. It is not likely that the wound stimulation due to beetle boring compensates for the lack of fungus. The number of spores carried by the beetle (lower than the number in the artificial inoculations) may explain the lack of role of L. wingfieldii in stimulating the tree’s defense reactions during T. piniperda attacks (Lieutier et al., 1989a, 1995). In some situations, the threshold of inoculation density is even higher than the threshold of attack density although the frequency of beetle infestation is below 100% (Guérard et al., 2000), thus emphasizing the crucial role of the beetles themselves. The nature of the elicitor is also unknown. It has been proposed to originate from the tree itself (Berryman, 1988; Lieutier, 1993) but that has never been demonstrated. 7.3. TREE DEATH A number of questions relate to this difficult problem: How is the tree killed? What are the respective roles of and the interactions among sapwood invasion by the fungus, release of fungal toxins, and decrease in water exchanges? What are the roles of fungi other than the blue staining ones? When do the fungi invade the sapwood? I proposed above that this invasion starts before the tree defenses are completely exhausted and then extends freely without constraint, but it seems also to occur after the water conductivity has decreased. However, the tree can recover and survive after a dramatic decrease of water conductivity if the fungus has not completely invaded the sapwood tissues (Guérard, Lieutier and Dreyer, unpublished). What is the chronology of events in the sapwood (drying, decrease of water conductivity, sapwood occlusion and fungus invasion)? What is the role of the sapwood defense mechanisms themselves in sapwood occlusion and tree killing? What is the role of the beetle and phloem invasion in the tree killing process? Kinetic experiments are needed that following the various events in the sapwood, in parallel to the development of the defense reactions and the success of beetle establishment in the phloem. Such studies must be done in situations close to (just below and above) the critical thresholds of attack / inoculation density, extending from the beginning of beetle attack until tree death is complete.

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7.4. EFFECTS ON THE AGGRESSORS The effects of tree resistance mechanisms on the aggressors are very poorly understood because most assays have been performed in vitro. The effects of terpenes, at least monoterpenes, on both the fungi and the beetles have been extensively investigated.. However, the role of the other secondary metabolites involved in the tree’s defenses, particularly phenols, is not understood. The effects of phenolic compounds on the blue stain fungi is a difficult problem, complicated by the fact that in vitro results seem opposite to results obtained in presence of wood (Hart and Shrimpton, 1979), but few Ophiostoma have been assayed in both situations. Bioassays with insects are difficult to carry out because of problems related to the stability of the compounds isolated from the tree reactions in presence of oxygen. Nevertheless, research is needed in this field because of the important qualitative and quantitative variations in these chemicals in relation to conifer defense mechanisms against bark beetles and their associated fungi (Brignolas et al., 1995a, 1998; Bois et Lieutier, 1997). 7.5. ENVIRONMENTAL FACTORS It is well known that the ability of a tree to resist beetle attacks depends on its’ vigour and environmental conditions (Safranyik et al., 1975; Berryman, 1976; Waring and Pitman, 1983; Raffa and Berryman, 1983a; Paine et al., 1984; Mullock and Christiansen, 1986). How environmental factors influence the tree – fungus bark beetle relationships is very poorly understood, however. They can act on the defense mechanisms themselves, on the fungi, or on the beetles. This very complex and difficult topic has been approached only relatively recently in most situations. Many studies of the effects of environmental factors, especially water stress and nitrogen fertilization, on defense mechanisms have been conducted (as examples, Paine and Stephen, 1987; Lorio, 1988; Paine et al., 1988; Dunn and Lorio, 1993; Christiansen, 1992; Christiansen and Glosli, 1996; Croisé et al., 1998b, 2001; Kyto et al., 1998; Viiri et al., 2001). Results are not presented here but they often lead to conflicting conclusions and various theories have been proposed to explain the observed effects (Lorio, 1986; Mattson and Haack, 1987; Lorio et al., 1990; Tuomi et al., 1991; Herms and Mattson, 1992; Koricheva et al., 1998 among others). Lombardero et al. (2001) suggested that these contradictions could be due to the fact that environmental factors may act in different ways on constitutive versus induced defenses. 7.6. TREE GENETIC FACTORS Genetic factors have also been studied relatively recently on clones and provenances with different resistance levels. Results not presented here, concerned preformed resistance (Nebeker et al., 1992) as well as induced defense (Ferrell et al., 1993; Ferrell and Otrosina, 1996; Brignolas et al., 1995b, 1998; Lieutier et al., 1996b;

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Bois and Lieutier, 1997, 2000; Franceschi et al., 1998; Nagy et al., 2000, among others). In some cases, predictors of tree resistance have been proposed (Brignolas et al, 1995a, 1998; Lieutier et al., 1996c; Bois and Lieutier, 1997). However, further research is needed in this field to yield practical applications (see below). 7.7. POPULATION ASPECTS Beetle population levels clearly play a decisive role in beetle establishment in relation to reaching the critical threshold of attack density (see references above). However, other population aspects, more related to the “quality” of the population, may also influence the tree – fungus - bark beetle relationships. For a given tree vigour, does the threshold of attack / inoculation density depend on the beetle population level? In other words, are outbreak populations intrinsically more aggressive or does their high aggressiveness results only from their high number of individuals? It has already been suggested that beetle pheromone production (Schlyter and Birgersson, 1989) and beetle host selection behaviour (Raffa, 1991) could vary with the population level. The percentage of beetles carrying fungus, and the ability of the fungus to stimulate tree defenses, could also depend on population levels. Since outbreak populations attack vigorous living trees, a high percentage of beetles with fungal spores can be expected in this case, as well as a high ability of the fungus to stimulate tree defenses, making the association more efficient in exhausting tree defenses. In non-outbreak populations, the number of beetles is too low to allow establishment on trees other than very weakened ones. Fungal associates are thus not an absolute necessity for the beetles to colonize trees. In such a case, the percentage of beetles vectoring fungi can be expected to stay at low levels, and the ability of the fungus to stimulate tree defenses would also remain low. In addition, fungus pathogenicity as well as fungus species composition could vary with beetle population levels (Solheim, 1992; 1993), and thus also contribute to increasing the aggressiveness of the beetle population. All these aspects, however, still need to be investigated. Studies on the genetic structure of the populations of beetles and fungi have never been developed in relation to tree resistance mechanisms, although some have considered the possible effect of the host on the population genetics of the beetles (see references below in VIII.2). This could be, however, an important factor to consider in the context of the adaptation of the aggressors to host resistance (see below). 8. SOME POTENTIAL APPLICATIONS OF CONIFER RESISTANCE TO BARK BEETLES A general overview of the possibilities for utilizing tree resistance to insects in forest pest management is presented in several other chapters of this book. As for other insect species, there are numerous potential applications of conifer resistance to bark beetles. I will focus on a few selected research topics only, those that I consider to be the most likely to yield practical applications at large scales in the context of forestry.

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8.1. TREE SELECTION FOR RESISTANCE This is the most classical application of research on tree resistance to insect attacks. It results from the existence of a genetically controlled intra-specific variability of the effectiveness of the mechanisms of resistance. In studies conducted on clones and provenances, predictors of resistance to bark beetles have already been proposed for Norway spruce and Scots pine (see references above and Heidger and Lieutier, this volume). These predictors are related to the phenolic content of the phloem. They can be present before the aggressions or neosynthesized in response to attacks but, in all cases, they are correlated with the critical threshold of attack density and the role of the hypersensitive reaction. Such predictors may be used as resistance markers in genetic breeding programs taking into account resistance to bark beetles in addition to other desirable characteristics of trees (Bastien, 1999; Heidger and Lieutier, this volume). However, further research is needed before this can be a practical and effective approach for use in such programs (Heidger and Lieutier, this volume). Selecting trees for resistance, however, involves a risk. Indeed, as mentioned by Raffa (1991), increasing the resistance of all trees in a stand can create an intense selective pressure for beetles able to overcome tree resistance, thus bearing the risk of further dramatic epidemics. This risk is classical in all programs concerned with genetic selection of plants for resistance to insects. Nevertheless, it might be less important for bark beetles than for other forest insects, because of their particular biology and because of the essential role of the hypersensitive reaction in conifer resistance to bark beetles. For example, suppose that the genetic modifications allowing a beetle to overcome tree resistance, and hence to become a “superaggressive” beetle, is an increase in its capacity to tolerate some tree secondary metabolite synthesized in the hypersensitive reaction. This is very likely what has the higher chance to occur since the hypersensitive reaction is the most common and important mechanism of resistance in most conifers to most bark beetles species. Two situations can be distinguished. With typical endemic populations of beetles, only very weakened or dead trees can be successfully colonized. Such trees do not exhibit any significant resistance because no or very little hypersensitive reaction can occur. No pressure for selecting super-aggressive individuals thus exists in endemic populations of bark beetles, contrary to situations with other insects where host resistance is due to constitutive compounds. During epidemic (outbreak) populations, because the percentage of pre-existing super-aggressive beetles is naturally very low, mass aggregation on living trees will necessarily involve both the super-aggressive beetles and the “normal” beetles. All will cooperate in overcoming tree resistance and the normal beetles will benefit from the presence of the super-aggressive beetles. The threshold of attack density may be lowered but probably not very much. After the success of the attacks, all beetle categories will be able to reproduce and, consequently, the percentage of super-aggressive individuals will not change in the whole beetle population. The super-aggressive individuals thus do not appear to be particularly favoured during the epidemic populations either, plus outbreak periods generally last for only a few beetle generations. For the proportion of super-aggressive beetles to

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increase in the population, it is necessary topresume, that in addition to the genetic modifications mentioned above, they respond to a more or less specific attraction during aggregation, or that their intrinsic biotic potential has increased. This is, of course, not impossible, but the chance for such phenomena to occur together is low. 8.2. ADAPTATION OF THE AGGRESSORS TO HOST RESISTANCE This field of research is relatively new but it should develop rapidly in the near future. One aspect results directly from selecting trees for resistance to bark beetles. The risk of adaptation exists with bark beetles controlled by induced resistance mechanisms, even if it is lower than with insects controlled by constitutive resistance. Before using tree resistance in large tree genetic breeding programs, it is thus important to understand the possible ways that bark beetles and their associated fungi could adapt to induced resistance. Another aspect is related to potential shifts by bark beetles and their associated fungi to new host species. This can result from accidental introductions of beetles and fungi to new areas or from voluntary introductions of exotic tree species for extensive plantations. These man made situations are rather common nowadays. The repeated accidental introductions and the establishment of T. piniperda from Europe in North America (Mattson et al., 1994) illustrate the first situation, when exotic beetles are accidentally introduced into a new region. The introductions of Douglas-fir (Pseudotsuga menziesii) from North America and the Atlantic cedar (Cedrus atlantica) from Morocco for plantations in Europe during the 20th century are examples of the second, when exotic host trees are deliberately introduced into new areas. Owing to its particular biology involving shoot feeding, T. piniperda has no competitor in the North American pines. Similarly, in Europe, Douglas-fir and cedar represent empty ecological niches and abundant and monospecific sources of food for several bark beetle species. In any of these situations however, no extensive damage due to bark beetles has been reported yet. The reasons for this are unknown but the resistance mechanisms of the hosts are certainly involved. Nevertheless, adaptation of the beetles and their associated fungi to the resistance of their potential new hosts cannot be discarded in the more or less near future. More generally, global change, by modifying climate parameters, will very likely result in modifications of the geographic distributions of bark beetle species since temperature is an important factor in their biology (Chararas, 1962). Species will thus get in contact with new tree populations and new tree species, leading to the situation described above on a wide scale. Foresters urgently need information allowing them to evaluate the risk of damage and the options available for forest protection. All the above considerations thus emphasize the necessity for developing research on the factors that allow beetles and fungi to adapt to tree resistance mechanisms. In this context, resistance should even be enlarged to host attraction and deterrence. Such studies depend on understanding the relationships between, on the one hand, the genetic structure of the populations of beetles and fungi and, on the other hand, host quality in general, that is host species, host populations, host physiological status, etc. Tentative steps in that direction have already been undertaken several years ago while considering

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different tree species attacked by the same beetle species, but without really succeeding in separating the geographic effect from the effect of the host species on the genetic structure of the beetle population (Bright and Stock, 1982; Sturgeon and Mitton, 1982). This research is presently expanding rapidly with the development of efficient molecular technics, especially for the beetles themselves (Sturgeon and Mitton, 1986; Langor and Spence, J.R., 1991; Kelley et al., 1999, 2000), but these programs should also consider the associated fungi. 8.3. EFFECT OF STRESS AND ENVIRONMENTAL FACTORS ON THE TREE – AGGRESSORS’ RELATIONSHIPS Effects of stresses and environmental factors on tree resistance mechanisms to bark beetles and their associated fungi, as well as on the aggressors themselves, is a wide and very important research topic to consider, especially in the present context of pollution and climatic changes. Practical applications concern risk prediction, as well as physiological improvement of trees by adapted silvicultural methods. Several investigations have already been conducted, but no general results or applications are available yet, mainly because of the complexity of the underlying physiological problems and the variety of the models (see above VII.5). Significant advancements in this field will be possible only through close cooperation among entomologists, pathologists, and tree physiologists who should coordinate such research. Regarding possible applications to silviculture, it has been underlined that there is generally a high degree of compatibility between enhancing tree resistance and forest management objectives, especially because of a positive relation between tree growth rate and resistance levels (Raffa, 1991). However, positive correlations between growth rate and resistance are not always true since some bark beetle species, such as D. micans, seem to prefer healthy trees (Grégoire, 1988). Moreover, some management tactics can favor bark beetle attacks, either directly or indirectly. As an example, thinning favours the pine processionary caterpillar Thaumetopoea pityocampa of pine (Géri, 1980), and their attacks weaken the trees, making them more susceptible to bark beetles. Thus, forest management tactics and the various forest pest problems must be considered as a whole system and not as separate parts. This corresponds to the philosophy of integrated pest management.

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Bannan, M.W. 1936. Vertical resin ducts in the secondary wood of the Abietinae. New Phytologist. 1147. Barras, S.J., & Perry, T. 1971. Gland cells and fungi associated with prothoracic mycangium of Dendroctonus adjunctus (Coleoptera: Scolytidae). Annals of the Entomological Society of America,, 64:123-26. Bastien, C. 1999. Improvement of Tree Resistance to Biotic Aggressions: the Geneticist Point of View. In. Physiology and Genetics of Tree-Phytophage Interactions, F. Lieutier, W.J. Mattson, M.R. Wagner (Eds.). Versailles: INRA Editions,. Berryman, A.A. 1969. Response of Abies grandis to attack by Scolytus ventralis (Coleoptera: Scolytidae). The Canadian Entomologist, 101, 1033-41. Berryman, A.A. 1972. Resistance of conifers to invasion by bark beetle fungus associations. BioScience 22,598-602. Berryman, A.A. 1976. Theoretical explanation of mountain pine beetle dynamics in lodgepole pine forests. Environmental Entomology, 5,1225-33. Berryman, A.A. 1982. Population Dynamics of Bark Beetles. In Bark Beetles in North American Conifers, J.B. Mitton, K.B. Sturgeon (Eds.). Austin: Univ. Texas,. Berryman, A.A. 1988. Towards a Unified Theory of Plant Defense. In Mechanisms of Woody Plant Defenses Against Insects: Search for Pattern, W.J. Mattson, J. Lévieux, C. Bernard-Dagan (Eds.). New York: Springer. Berryman, A.A., & Ashraf, M. 1970. Effects of Abies grandis resin on the attack behavior and brood survival of Scolytus ventralis (Coleoptera: Scolytidae). The Canadian Entomologist, 102,1229-36. Berryman, A.A., & Ferrell, G.T. 1988. The Fir Engraver Beetle in Western States. In. Dynamics of Forest Insect Populations: Patterns, Causes, Implications, A.A. Berryman, ed. New York: Plenum Press. Birgersson, G., & Bergström, G. 1989. Volatiles released from individual spruce bark beetle entrance holes. Quantitative variations during the first week of attack. Journal of Chemical Ecology, 15, 246583. Blanche, C.A., Lorio, P.L. Jr., Sommers, R.A., Hodges, J.D., & Nebeker, T.E. 1992. Seasonal cambial growth and development of loblolly pine: xylem formation, inner bark chemistry, resin ducts, and resin flow. Forest Ecology and Management, 49,151-65. Bois, E., & Lieutier, F. 1997. Phenolic response of Scots pine clones to inoculation with Leptographium wingfieldii, a fungus associated with Tomicus piniperda. Plant Physiology and Biochemistry, 35, 819-25. Bois, E., & Lieutier, F. 1999. Histological Observations on the Interaction Between Leptographium wingfieldii Morelet and Pinus sylvestris L. In. Physiology and Genetics of Tree-Phytophage Interactions, F. Lieutier, W.J. Mattson, M.R. Wagner, (Eds.). Versailles: INRA Editions. Bois, E., & Lieutier, F. 2000. Resistance level of Scots pine clones to artificial introductions of Tomicus piniperda (Col. : Scolytidae) and Leptographium wingfieldii (Deuteromycetes). Journal of Applied Entomology, 124,163-67. Bois E., Lieutier F., & Yart, A. 1999. Bioassays on Leptographium wingfieldii, a bark beetle associated fungus, with phenolic compounds of Scots pine phloem. European Journal of Plant Pathology, 105,51-60. Bordasch, R.P., & Berryman, A.A. 1977. Host resistance to the fir engraver beetle Scolytus ventralis (Coleoptera: Scolytidae). 2. Repellence of Abies grandis resins and some monoterpenes. The Canadian Entomologist., 109,95-100. Bridges, J.R. 1987. Effects of terpenoïd compounds on growth of symbiotic fungi associated with the southern pine beetle. Phytopathology, 77,83-85. Bridges, J.R., Nettleton, W.A., & Conner, M.D. 1985. Southern pine beetle (Coleoptera: Scolytidae) infestations without the blue-stain fungus, Ceratocystis minor. Journal of Economic Entomology, 78,325-27. Bright, D.E., & Stock, M.W. 1982. Taxonomy and Geographic Variations. In. Bark Beetles in North American Conifers, J.B. Mitton, K.B. Sturgeon (Eds.). Austin: University of Texas. Brignolas, F. Rôle 1995. des composés phénoliques dans l’efficacité de la réaction induite du liber de l’épicea (Picea abies) à enrayer la progression d’Ophiostoma polonicum, champignon associé au Scolytide Ips typographus. Thèse Univ. Orléans: Physiologie et biologie des organismes, populations, interactions.

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Cook, S.P., & Hain, F.P. 1985. Qualitative examination of the hypersensitive response of loblolly pine Pinus taeda L., inoculated with two fungal associates of the southern pine beetle, Dendroctonus frontalis Zimmermann (Coleoptera: Scolytidae). Environmental Entomology, 14, 396-400. Coyne, J.F., & Lott, L.H. 1976. Toxicity of substances in pine oleoresin to southern pine beetle. J. Ga. Entomol. Soc., 11, 297-301. Croisé, L., Lieutier, F., Dreyer, E. 1998a. Scots pine responses to number and density of inoculation points with Leptographium wingfieldii Morelet, a bark beetle-associated fungus. Ann. Sci. For., 55, 497-506. Croisé, L., Dreyer, E., & Lieutier, F. 1998. Effects of drought stress and severe pruning on the reaction zone induced by single inoculations with a bark beetle associated fungus (Ophiostoma ips) in the phloem of young Scots pines. Canadian Journal of Forest Research, 28, 1814-24. Croisé, L., Lieutier, F., Cochard, H., & Dreyer, E. 2001. Effects of drought stress and high density stem inoculations with Leptographium wingfieldii on hydraulic properties of young Scots pine trees. Tree Physiology, 21, 427-36. Croteau, R., Burbott, A.J., & Loomis, W.D. 1972. Apparent energy deficiency in mono- and sesquiterpene biosynthesis in peppermint. Phytochemistry, 11, 2937-48. Croteau, R., & Loomis, W.D. 1975. Biosynthesis and metabolism of monoterpenes. Int. Flavours Food Addit., 6, 292-96. DeAngelis, J.D., Nebeker, T.E., & Hodges, J.D. 1986. Influence of tree age and growth rate on the radial resin duct system in loblolly pine (Pinus taeda). Canadian Journal of Botany, 64, 1046-49. Delorme, L., & Lieutier, F. (1990). Monoterpene composition of the preformed and induced resins of Scots pine, and their effect on bark beetles and associated fungi. Eur. J. For. Pathol., 20, 304-16. Dunn, J.P., & Lorio, P.L. Jr. 1992. Effect of bark girdling on carbohydrate supply and resistance of loblolly pine to southern pine beetle (Dendroctonus frontalis Zimm.) attack. Forest Ecology and Management, 50, 317-30. Dunn, J.P., & Lorio, P.L. Jr. 1993. Modified water regimes affect photosynthesis, xylem water potential, cambial growth, and resistance of juvenile Pinus taeda L. to Dendroctonus frontalis (Coleoptera: Scolytidae). Environmental Entomology, 22, 948-57. Evensen, P.C., Solheim, H., Hoiland, K., & Stenersen, J. 2000. Induced resistance of Norway spruce, variation of phenolic compounds and their effects on fungal pathogens. Forest Pathology, 30, 97-108. Everaerts, C., Grégoire, J.-C., & Merlin, J. 1988. Toxicity of Spruce Monoterpenes Against Bark Beetles and Their Associates . In. Mechanisms of Woody Plant Defenses Against Insects: Search for Pattern, W.J. Mattson, J. Lévieux, C. Bernard-Dagan (Eds.). New York: Springer. Ferrell, G.T. 1983. Host resistance to the fir engraver, Scolytus ventralis (Coleoptera: Scolytidae): frequencies of attacks containing resin blisters and canals of Abies concolor. Canadian Entomologist, 115, 1421-28. Ferrell, G.T., Otrosina, W.J., & DeMars, C.J. Jr. 1993. Assessing the susceptibility of white fir to the fir engraver, Scolytus ventralis LeC. (Coleoptera: Scolytidae), using fungal inoculation. Canadian Entomologist, 125, 895-901. Ferrell, G.T., & Otrosina, W.J. 1996. Differential Susceptibility of White Fir Provenances to the Fir Engraver and its Fungal Symbiont in Northern California . In. Dynamics of Forest Herbivory: Quest for Pattern and Principle, W.J. Mattson, P. Niemela, M. Rousi (Eds.). USDA Forest Service General Technical Report NC-183. Franceschi, V.R., Krekling, T., Berryman, A.A., & Christiansen, E. 1998. Specialized phloem parenchyma cells in Norway spruce (Pinaceae) bark are an important site of defense reactions. American Journal of Botany 85, 601-15. Franceschi, V.R., Krokene, P., Krekling, T., Berryman, A.A., & Christiansen, E. 2000. Phloem parenchyma cells are involved in local and distant defense responses to fungal inoculation or bark beetle attack in Norway spruce (Pinaceae). American Journal of Botany, 87, 314-26. Gambliel, H., Gates, R.G., Caffey-Moquin, & Paine, T.D. 1985. Variation in the Chemistry of Loblolly Pine in Relation to Infection by the Blue-Stain Fungus . In. Integrated Pest Management Research Symposium: The procedings, S.J. Branham, R.C. Thatcher (Eds.). New Orleans: USDA Forest Servervice General Technical Report SO-56. Géri, C. 1980. Application des méthodes démécologiques aux insectes défoliateurs forestiers. Cas de Diprion pini L. (Hyménoptère Diprionidae). Dynamique des po^ulations de la processionnaire du Pin Thaumetopoea pytiocampa Schiff. (Lepidoptère Thaupetopoeidae) dans l’île de Corse. Thèse Univ. Paris Sud Orsay.

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Kyto, M., Niemela, P., Annila, E. 1996. Vitality and bark beetle resistance of fertilized Norway spruce. Forest Ecology and Management, 84, 149-57. Kyto, M., Niemela, P., & Annila, E. 1998. Effects of vitality fertilization on the resin flow and vigour of Scots pine in Finland. Forest Ecology and Management, 102, 121-30. Langor, D.W., & Spence, J.R. 1991. Host effect on allozyme and morphological variation of the mountain pine beetle, Dendroctonus ponderosae Hopkins (Coleoptera: Scolytidae). Canadian Entomologist, 123, 395-410. Langström, B., & Hellqvist, C. 1993. Induced and spontaneous attacks by pine shoot beetles on young Scots pine trees: tree mortality and beetle performances. Journal of Applied Entomology, 115, 25-36. Langström, B., Hellqvist, C., Ericsson, A., & Gref, D. 1992. Induced defense reaction in Scots pine following stem attacks by Tomicus piniperda L. Ecography, 15, 318-27. Langström, B., Solheim, H., Hellqvist, C., Gref, D. 1993. Effects of pruning young Scots pines on host vigour and susceptibility to Leptographium wingfieldii and Ophiostoma minus, two blue-stain fungi associated with Tomicus piniperda. Eur. J. For. Pathol., 23, 400-15. Lewinsohn, E., Gijzen, M., & Croteau, R. 1991. Defense mechanisms of conifers: relationship of monoterpene cyclase activity to anatomical specialization and oleoresin monoterpene content. Plant Physiology, 96, 38-43. Lewinsohn, E., Gijzen, M., Croteau, R. 1991. Defense mechanisms of conifers: differences in constitutive and wound-induced monoterpene biosynthesis among species. Plant Physiology, 96, 44-49. Lieutier, F. 1992. Les réactions de défense des conifères et stratégies d’attaques de quelques Scolytides européens. Mem. Soc. R. Beige Entomol. 35, 529-539. Lieutier, F. 1993. Induced Defense Reaction of Conifers to Bark Beetles and Their Associated Ophiostoma Species. In. Ceratocystis and Ophiostoma. Taxonomy, Ecology, and Pathogenicity, M.J. Wingfield, K.A. Seifert, J.F. Webber (Eds.). Saint Paul: APS Press,. Lieutier, F. 1995. Associated Fungi, Induced Reaction and Attack Strategy of Tomicus Piniperda (Coleoptera: Scolytidae) in Scots Pine. In. Behavior, Population Dynamics and Control of Forest Insects , F.P. Hain, S.M. Salom, W.F. Ravlin, T.L. Payne, K.F. Raffa (Eds.). Proc. Intern. Union For. Res. Organizations Joint Conf. 1994 February 6-11 Maui, Hawaï. Lieutier, F., & Berryman, A.A. 1988a. Preliminary histological investigations on the defense reactions of three pines to Ceratocystis clavigera and two chemical elicitors. Canadian Journal of Forest Research, 18, 1243-47. Lieutier, F., & Berryman, A.A. 1988b. Elicitation of Defensive Reactions in Conifers. In. Mechanisms of Woody Plant Defenses Against Insects: Search for Pattern, W.J. Mattson, J. Lévieux, C. BernardDagan (Eds.). New York: Springer,. Lieutier, F., Berryman, A.A., & Millstein, J.A. 1991b. Preliminary study of the monoterpene response of three pines to Ophiostoma clavigerum (Ascomycetes: Ophiostomatales) and two chemical elicitors. Ann. Sci. For., 48, 377-88. Lieutier, F., Brignolas, F., Picron, V., Yart A., & Bastien, C. 1996c. Can Phloem Phenols Be Used as Markers of Scots Pine Resistance to Bark Beetles ? In. Dynamics of Forest Herbivory: Quest for Pattern and Principle, W.J. Mattson, P. Niemela, M. Rousi (Eds.). USDA Forest Service General Technical Report NC-183,. Lieutier, F., Cheniclet, C., & Garcia, J. 1989a. Comparison of the defense reactions of Pinus pinaster and Pinus sylvestris to attacks by two bark beetles (Coleoptera: Scolytidae) and their associated fungi. Environmental Entomology, 18, 228-34. Lieutier, F., Garcia, J., Romary, P., & Yart, A. 1995. Wound reactions of Scots pine (Pinus sylvestris L.) to attacks by Tomicus piniperda L. and Ips sexdentatus Boern. (Coleoptera: Scolytidae). Journal Applied. Entomology, 119, 591-600. Lieutier, F., Garcia, J., Yart, A., Vouland, G., Pettinetti, M., & Morelet, M. 1991c. Ophiostomatales (Ascomycètes) associées à Ips acuminatus Gyll (Coleoptera: Scolytidae) sur le Pin sylvestre (Pinus sylvestris L.) dans le Sud-Est de la France et comparaison avec Ips sexdentatus Boern. Agronomie, 11, 807-17. Lieutier, F., Langström, B., Solheim, H., Hellqvist, C., & Yart, A. 1996b. Genetic and Phenotypic Variation in the Induced Reaction of Scots Pine, Pinus Sylvestris L., to Leptographium Wingfieldii: Reaction Zone Length and Fungal Growth . . In. Dynamics of Forest Herbivory: Quest for Pattern and Principle, W.J. Mattson, P. Niemela, M. Rousi (Eds.). USDA Forest Service General Technical Report NC-183,.

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Lieutier, F., Sauvard, D., Brignolas, F., Picron, V., Yart, A., Bastien, C., & Jay-Allemand, C. 1996a. Changes in phenolic metabolites of Scots-pine phloem induced by Ophiostoma brunneo-ciliatum, a bark-beetle-associated fungus. Eur. J. For. Pathol., 26, 145-58. Lieutier, F., Vouland, G., Pettinetti, M., Garcia, J., Romary, P., & Yart, A. 1992. Defense reactions of Norway spruce (Picea abies Karst.) to artificial insertion of Dendroctonus micans Kug. (Col. Scolytidae). Journal Applied Entomology 114, 174-86. Lieutier, F., Yart, A., Garcia, J., & Ham, M-C. 1990. Cinétique de croissance des champignons associés à Ips sexdentatus Boern et à Tomicus piniperda L. (Coleoptera: Scolytidae) et des réactions de défense des pins sylvestres (Pinus sylvestris L.) inoculés. Agronomie, 10, 243-56. Lieutier, F., Yart, A., Garcia, J., Ham, M-C., Morelet, M., & Lévieux, J. 1989b. Champignons phytopathogènes associés à deux Coléoptères Scolytidae du Pin sylvestre (Pinus sylvestris L.) et étude préliminaire de leur agressivité envers l’hôte. Ann Sci. For., 46, 201-216. Lieutier, F., Yart, A., Garcia, J., Poupinel, B., & Lévieux, J. 1988. Do Fungi Influence the Establishment of Bark Beetles in Scots Pine ? In. Mechanisms of Woody Plant Defenses Against Insects: Search for Pattern, W.J. Mattson, J. Lévieux, C. Bernard-Dagan (Eds.). New York: Springer. Lieutier, F., Yart, A., Jay-Allemand, C., & Delorme, L. 1991a. Preliminary investigations on phenolics as a response of Scots pine phloem to attacks by bark beetles and associated fungi. Eur. J. For. Pathol., 21, 354-54. Lombardero, M.J., Ayres, M.P., Lorio, P.L. Jr., & Ruel, J.J. 2001. Environmental effects on constitutive and inducible resin defenses of Pinus taeda. Ecol. Lett., in press. Loman, A.A. Bioassays of fungi isolated from Pinus contorta var. latifolia with pinosylvin, pinosylvinmonomethyl ether, pinobanksin, and pinocembrin. Canadian Journal of Botany, 48, 130308. Lorio, P.L. Jr. 1986. Growth-differentiation balance: a basis for understanding southern pine beetle-tree interactions. Forest Ecology and Management, 14, 259-73. Lorio, P.L. Jr. Growth and Differentiation-Balance Relationships in Pines Affect Their Resistance to Bark Beetles (Coleoptera: Scolytidae) . In. Mechanisms of Woody Plant Defenses Against Insects: Search for Pattern, W.J. Mattson, J. Lévieux, C. Bernard-Dagan (Eds.). New York: Springer, 1988. Lorio, P.L. Jr., Sommers, R.A., Blanche, C.A., Hodges, J.D., & Nebeker, T.E. 1990. Modelling Pine Resistance to Bark Beetles Based on Growth and Differentiation Balance Principles . In. Process Modelling of Forest Growth Responses to Environmental Stress, R.K. Dixon, R.S. Meldahl, G.A. Ruark, W.G. Warren (Eds.). Portland, Oreg.: Timber press,. Lorio, P.L. Jr., Stephen, F.N., & Paine, T.D. 1995. Environment and ontogeny modify loblolly pine response to induced acute water deficits and bark beetle attack. Forest Ecology and Management, 73, 97-110. Matson, P.A., & Hain, F.P. 1985. Host Conifer Defense Strategies: a Hypothesis. In. The Role of the Host in the Population Dynamics of Forest Insects: Proc. IUFRO Conf., L. Safranyik ed. Victoria: Can. For. Serv. Pac. For. Res. Cent.,. Mattson, W.J., & Haack, R.A. 1987. The role of drought in outbreaks of plant-eating insects. Bioscience, 37, 110-18. Mattson, W.J., Lawrence, R.K., Haack, R.A., Herms, D.A., & Charles, P.J. 1988. Defensive Strategies of Woody Plants Against Different Insect-Feeding Guilds in Relation to Plant Ecological Strategies and Intimacy of Association with Insects. In. Mechanisms of Woody Plant Defenses Against Insects: Search for Pattern, W.J. Mattson, J. Lévieux, C. Bernard-Dagan (Eds.). New York: Springer,. Mattson, W.J., Niemela P., Millers, L., & Inguanzo, Y. 1994. Immigrant phytophagous insects on woody plants in the United States and Canada: An annotated list. USDA Forest Service General Technical Report NC-169. Miller, R.H., & Berryman, A.A. 1986. Nutrient allocation and mountain pine beetle attack in girdled lodgepole pines. Canadian Journal of Forest Research, 16, 1036-40. Müllick, D.B. 1977. The non-specific nature of defense in bark and wood during wounding, insect, and pathogen attack. Recent advances in phytochemistry, 11, 359-441. Mulock, P., Christiansen E. The threshold of successful attack by Ips typographus on Picea abies: a field experiment. Forest Ecology and Management, 1986 14, 125-132. Nagy, N.E., Franceschi, V.R., Solheim, H., Krekling, T., Christiansen E. Wound-induced traumatic resin duct development in stems of Norway spruce (Pinaceae): anatomy, and cytological traits. American Journal of Botany, 2000 87:302-13.

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CHAPTER 3 MECHANISMS OF RESISTANCE IN TREES TO DEFOLIATORS

KAREN M. CLANCY

USDA Forest Service Research and Development, Rocky Mountain Research Station, Southwest Forest Science Complex, 2500 South Pine Knoll Drive Flagstaff, AZ 86001-6381 USA 1. INTRODUCTION Insects that feed on the foliage of trees (i.e., defoliators or folivores) include species in the orders Lepidoptera, Hymenoptera, Coleoptera, Diptera, Orthoptera, and Phasmida (Barbosa & Wagner, 1989). The most renowned forest defoliators are species that are characterized by periodic population outbreaks, such as the gypsy moth (Lymantria dispar) and tussock moths in the family Lymantriidae, spruce budworms (Choristoneura species) in the family Tortricidae, and the pine butterfly (Neophasia menapia) in the family Pieridae. All of these species are lepidopterans. Some hymenopterans can also cause widespread defoliation of trees, such as the pine sawflies (Neodiprion species) in the family Diprionidae. There are also species of phasmids (i.e., walking sticks) that are occasionally important defoliators in hardwood forests. At least 10 mechanisms are known to be important in resistance of trees to insect defoliators. Many of these mechanisms are not independent of one another, and it is likely that linked suites of mechanisms interact in determining host plant resistance to insect folivores. 1.1 PHENOLOGICAL ASYNCHRONY BETWEEN HOST TREES AND THEIR INSECT HERBIVORES This is often an important mechanism of resistance for species that are early-season feeders on the expanding new buds and leaves of trees; early or late bud burst can directly affect both the quantity and quality of suitable food available to herbivores at specific times (Quiring, 1992; Lawrence et al., 1997). If emergence of larvae or 79 M.R. Wagner et al. (eds.), Mechanisms and Deployment of Resistance in Trees to Insects, 79–103. © 2002 Kluwer Academic Publishers. Printed in the Netherlands.

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nymphs is too early in relation to budburst of host trees, the insects will be forced to disperse to find suitable food resources. Increased dispersal invariably leads to higher mortality from natural enemies or starvation. Alternatively, if insect emergence is too late, folivores will be forced to feed on leaves or needles that are too mature to be an optimal food source; this can result in slower larval growth rates, smaller (and less fecund) adults, and increased larval mortality. 1.2 HOST TREE TOLERANCE OF DEFOLIATION The ability to simply tolerate defoliation can also confer resistance to some insect defoliators (sensu Painter’s [1958] definition). This mechanism is frequently associated with inherently higher growth rates of the trees, or increased tree vigor (but also see Price [1991]). 1.3 HOST TREE COMPENSATORY PHOTOSYNTHESIS AND GROWTH Trees commonly respond to defoliation via compensatory growth, which involves stimulation of photosynthesis, increased leaf nitrogen, and greater allocation of carbohydrate reserves to growth of new foliage instead of roots (Clancy et al., 1995). Increased rates of photosynthesis and growth in response to insect herbivory, or compensatory photosynthesis and growth, can help promote tree recovery from defoliators. Although most plants compensate for herbivory to some extent, the degree of compensation varies widely (Trumble et al., 1993). Differences in photosynthetic compensation among individual trees of the same species have not been widely evaluated as a mechanism of tree resistance to insect herbivory (Chen et al., 2001 a). 1.4 TOUGHNESS OF LEAVES AND NEEDLES Tough leaves or needles can be an important deterrent to some insect folivores. For example, ponderosa pine (Pinus ponderosa) trees with tougher needles were more resistant to attack by Neodiprion fulviceps sawflies (Wagner & Zhang, 1993). Needle toughness negatively influenced the feeding success of sawfly larvae (Wagner & Zhang, 1993), and it may also have caused increased wear on the sawlike ovipositor of the females as they inserted their eggs into mature needles (M. R. Wagner, personal communication). Lawrence et al. (1997) concluded that needle toughness was an important factor in defining the “phenological window of susceptibility” for spruce budworm (Choristoneura fumiferana) feeding on white spruce (Picea glauca); this example emphasizes the linkage between host plant phenology and needle toughness.

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1.5 LOW NUTRITIVE QUALITY OF FOLIAGE Plant tissues that do not provide a good match to the defoliator’s requirements for protein, carbohydrates, or minerals can reduce growth rates of larvae and cause lower rates of reproduction in the adults. Survival rates of all life stages, including eggs, can also be reduced. However, Larsson (Chapter 1 of this volume) noted that “Because there is so much variation that is seemingly of ontogenetic and physiological origin primary metabolites are rarely considered to be part of plant resistance, although this may be erroneous.” Hanover (1975) also observed that “although resistance mechanisms involving host nutritional status may actually be quite prevalent, they are most difficult to prove because the net effect is likely to be more quantitative or subtle than that of the other resistance types.” 1.6 DEFENSIVE COMPOUNDS IN FOLIAGE Larsson (Chapter 1 [section 3.2] of this volume) presented a good summary of the role of secondary metabolites as resistance traits. Host plant defensive compounds (or allelochemicals) that are always present in leaves or needles are known as constitutive (or preformed) defenses. These constitutive defensive compounds in foliage can function as digestibility reducers or toxins for insect defoliators, or they may act as feeding or oviposition deterrents. 1.7 INDUCED DEFENSES IN HOST TREES Induced resistance may also include host plant allelochemicals, but in this case defensive chemicals are produced in response to defoliation, and they increase the tree’s resistance to subsequent herbivory in the short- or long-term. Induced resistance can also include changes in foliar nutrients, leaf toughness, or other characteristics that increase the tree’s resistance to folivores. Larsson (Chapter 1[section 5] of this volume) discussed induced resistance, and noted that coniferous trees seem to be less prone to induced defenses following defoliation by insects than are deciduous trees. Toumi et al. (1988) suggested that the difference might be explained by different carbon allocation strategies – deciduous trees have large carbohydrate reserves in their roots, whereas coniferous trees store most of their carbohydrates in the evergreen needles they retain for multiple years. 1.8 INDUCED SUSCEPTIBILITY IN HOST TREES Some host trees become better sources of food for insect defoliators with successive years of defoliation; changes can occur in concentrations or balances of foliar nutrients or defensive compounds, or in other traits such as growth rates or phenology of bud break. For example, McMillin & Wagner (1997) concluded that ponderosa pine trees that were chronically defoliated by Neodiprion autumnalis sawflies became better sources of food for the sawfly larvae via decreased ability of

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the trees to produce carbon-based defensive chemicals and improved foliar nitrogen, resulting in a positive feedback loop. On the other hand, trees that do not exhibit this type of induced change in foliar chemistry etc. will be more resistant to damage from defoliators over the long-run. 1.9 THREE-TROPHIC-LEVEL INTERACTIONS A more complicated mechanism of resistance involves three-trophic-level interactions among host trees, their insect folivores, and natural enemies of the defoliators, an idea first proposed by Price et al. (1980). Larsson (Chapter 1 [sections 7 and 8] of this volume) covers this topic in more detail. The basic concept is that characteristics of some host trees may increase susceptibility of the insect defoliators to predators, parasites, or pathogens. On the other hand, insects can also exploit host plant traits to help defend themselves against natural enemies, so tri-trophic interactions can also end up benefiting the insect herbivores in some cases. 1.10 HOST TREE MICROBIAL MUTUALISTS Finally, another complex mechanism of resistance may include host tree microbial mutualists such as mycorrhizae or fungal endophytes (see Saikkonen & Neuvonen [1993] for an overview). Ectomycorrhizal fungi improve a tree’s ability to obtain water and nutrients such as nitrogen and phosphorus from the soil, in exchange for simple sugars they extract from the trees’ feeder roots for nourishment (Molina et al., 1993; Mathiasen & Albion, 2001). Gehring & Whitham (1991) demonstrated that high levels of insect herbivory could reduce the ability of pinyon pine (Pinus edulis) trees to support ectomycorrhizal symbioants. It is possible that ectomycorrhizal mutualists can also influence the resistance of host trees to insect defoliators via effects on the tree’s growth rates or foliar biochemistry. In other words, perhaps trees that are inherently better hosts for ectomycorrhizae are more resistant to insect defoliators because of the benefits the trees gain from this symbiosis. The fungal endophytes that are ubiquitously present in leaves and needles may also enhance host tree resistance to insect folivores through the action of deterrent or toxic compounds they produce (Saikkonen et al., 1998). 2. MECHANISMS OF RESISTANCE OF DOUGLAS-FIR TREES TO THE WESTERN SPRUCE BUDWORM My collaborators and I have investigated the potential role of most of these mechanisms using the western spruce budworm (Choristoneura occidentalis) and Douglas-fir (Pseudotsuga menziesii var. glauca) as a model system. We choose to study this insect-plant system in detail because the budworm is the most important forest defoliator in western North America (Brookes et al., 1987), and Douglas-fir is

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a commercially important host tree species (Silen 1978; Hermann & Lavender, 1990; Hardin et al., 2001). The remainder of this chapter summarizes what we know about mechanisms of resistance of Douglas-fir to damage from the western spruce budworm. I have not investigated the role of three-trophic-level interactions in this system, so I will not present any information on this potentially very important mechanism. The various mechanisms of resistance reported below were evaluated using a combination of laboratory and greenhouse experiments, plus field observations on 40 pairs of mature Douglas-fir trees that are phenotypically resistant versus susceptible to damage from the budworm (Clancy, 2001). Three-generation laboratory diet bioassays (Clancy, 1991b) were used to quantify the budworm’s nutritional niche with regard to levels of nitrogen (Clancy, 1992a), sugars (Clancy, 1992b), minerals (Clancy & King, 1993; unpublished data), and monoterpenes (Clancy et al., 1992; Clancy, 1993; unpublished data) that occur in Douglas-fir foliage. The budworm’s response curves from the diet bioassays were compared to levels of the nutrients and terpenes in current-year foliage from pairs of Douglas-fir trees that appeared to be “resistant” versus “susceptible” to western spruce budworm defoliation. Twelve pairs of trees on the Pike National Forest (NF) in Colorado were sampled in 1988, 1989, and 1990; the trees were 45-123 years old when annual growth rings were counted on increment cores collected in 1990 (Clancy, 199la; Clancy et al., 1993). Another 12 pairs of trees on the Kaibab NF in Arizona were sampled in 1989 and 1990; the trees were 67-115 years old in 1990 (Clancy et al., 1993). Sixteen pairs of trees on the San Isabel NF in Colorado were sampled in 1995 and 1996; the trees were 37-118 years old in 1995 (Clancy, 2001). Most of the trees from the Pike and Kaibab NF sites were successfully cloned (by whip grafting) in 1991 and 1992. Clones from 12 pairs of trees from these two sites were used in greenhouse experiments in 1998 and 1999 (Chen, 2001). Chen et al. (2001a) also grew half-sib seedling progeny from 13 of the 40 pairs of trees to use in greenhouse studies. Finally, Chen et al. (2001b) established that there are genetically-based differences between the resistant and susceptible parent trees, suggesting that the phenotypic differences observed in resistance of these interior Douglas-firs to budworm defoliation are at least partly caused by genetic differences among trees. 2.1 PHENOLOGICAL ASYNCHRONY BETWEEN DOUGLAS-FIRS AND THE WESTERN SPRUCE BUDWORM Variation in bud phenology is particularly important for early-season feeders like the western spruce budworm. Budworm larvae can damage all types and developmental stages of tissues (Frank & Jenkins, 1986), but they prefer to feed on nutrient-rich tissues such as swollen buds, current-year needles, and pollen (Shepherd, 1992; Dodds et al., 1996). Budworm larvae can also feed on less nutritious older needles as a survival strategy until swollen buds and new needles are available (Shepherd, 1992).

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Several lines of evidence suggest that differences in bud break phenology are an important mechanism of resistance in Douglas-fir trees. First, field observations of bud break phenology of paired resistant and susceptible trees clearly showed that the resistant trees consistently had later budburst phenology than the susceptible trees ( Table 1) (Clancy et al., 1993).

Second, current-year buds on the susceptible clones flushed earlier than those on the resistant clones, when the trees were grown in a common environment in greenhouses (Chen et al., 2001a). These results support a genetic basis for the differences I observed in bud break phenology in the field. Phenology of bud break is known to be a highly heritable trait in Douglas-fir (Silen, 1978). Third, Chen (2001) reared western spruce budworm larvae on resistant and susceptible clones in greenhouse bioassay experiments to establish how host tree phenotype affected budworm survival and reproduction. Two different bioassays were used to assess the importance of bud burst phenology as a factor determining host plant resistance. In the 1988 experiment, budworm feeding was matched to the bud flush of each individual plant. Larvae reared on the resistant clones had 1.7 times greater realized fitness (i.e., number of larvae produced) compared to those reared on the susceptible clones (Fig. 1). In the 1999 experiment, budworm feeding was matched to bud flush of the whole population of plants. The susceptible clones had an earlier budburst phenology compared to the resistant clones, which mimicked the pattern observed for the parent trees in the field. In this case, budworm larvae

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reared on the susceptible clones had 1.4 times higher realized fitness than budworms reared on the resistant clones (Fig. 1). Chen (2001) concluded that western spruce budworm survival and reproduction is indeed better on susceptible phenotypes of Douglas-fir under conditions similar to those that the insects and trees experience in the field. Moreover, the results confirmed that variation among trees in budburst phenology is an important mechanism of resistance influencing interactions between the budworm and its Douglas-fir host trees.

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Fourth, Chen et al. (2001a) also discovered in the 1998 greenhouse bioassay experiment that when larvae were placed on each grafted tree when buds were highly suitable for feeding, the resistant clones were defoliated more than the susceptible clones However, in the 1999 experiment, when larvae were placed on all trees on the same date regardless of bud burst stage, resistant clones were defoliated less than susceptible clones Thus, budworm defoliation of clones depended on the degree of synchrony between bud burst phenology and budworm larval feeding. 2.2 DOUGLAS-FIR TOLERANCE OF BUDWORM DEFOLIATION, AND THE ROLE OF HOST TREE VIGOR Trees that have inherently greater growth rates may be able to tolerate the loss of needles (i.e., photosynthetic capacity) to budworm defoliation without experiencing as much physiological stress as more slowly growing trees do (Chen et al. 2001a). In general, the evidence indicates that mature Douglas-fir trees that are resistant to budworm damage tend to have greater growth rates than susceptible trees do. Furthermore, open pollinated seedlings from resistant trees also have higher growth rates than seedlings from susceptible trees, implying there is a genetic basis for the difference. I evaluated this mechanism for mature trees in the field by comparing radial growth rates of the 40 paired resistant and susceptible trees. Five-year radial growth increments were measured on increment cores collected from the trees. The resistant trees at the Pike and Kaibab National Forest sites appeared to be more vigorous than the susceptible trees – they had sustained less impact on their radial growth from budworm defoliation compared to the susceptible trees (P < 0.001; Table 2) (Clancy et al., 1993). This implies that resistant trees may be more tolerant of defoliation because they can compensate better for photosynthetic area lost from herbivory. Overall, the resistant trees at the Pike and Kaibab sites had 1.48 times greater radial growth than the susceptible trees did from 1966-1990. However, this pattern was not consistent across all three sites. There were no detectable differences in radial growth increments between the resistant and susceptible trees at the San Isabel National Forest site from 1970-1994 ( Table 2).

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Chen et al. (2001a) grew half-sib seedlings from open-pollinated seeds collected from 13 of the 40 pairs of resistant and susceptible mature trees (i.e., 26 families). In the absence of budworm defoliation, height and base diameter of half-sib seedlings from resistant trees were significantly greater compared with seedlings from susceptible trees in all 3 years of growth in a greenhouse (P < 0.001); total biomass of the resistant seedlings was also greater in years 2 and 3 (P < 0.001) (Chen et al., 2001a). The authors concluded that resistant trees were genetically

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predisposed to grow faster than susceptible trees, and suggested that inherently higher growth rate may promote tree resistance or recovery from budworm defoliation by rapid regrowth. 2.3 DOUGLAS-FIR COMPENSATORY PHOTOSYNTHESIS AND GROWTH IN RESPONSE TO BUDWORM DEFOLIATION Chen et al. (2001a) hypothesized that clones of resistant Douglas-firs would respond to budworm defoliation with a greater increase in net photosynthetic rate than clones of susceptible trees, but they concluded that this hypothesis was not supported in greenhouse bioassay experiments. There was evidence of a stronger compensatory photosynthetic response to defoliation in resistant compared to susceptible clones after 1 year of defoliation in the 1998 bioassay, when the resistant clones were defoliated more than the susceptible clones (see Fig. 1 for details regarding the bioassays). However, in the 1999 bioassay, the susceptible clones were defoliated more, resulting in similar cumulative defoliation of the resistant and susceptible clones over 2 years, and similar responses in terms of compensatory photosynthesis in the 1999 bioassay measurements. Chen et al. (2001a) noted, “Because late bud burst phenology apparently enabled resistant trees to avoid heavy budworm defoliation, there is probably little selection for mechanisms leading to compensatory photosynthesis in resistant genotypes”. 2.4 TOUGHNESS OF DOUGLAS-FIR NEEDLES It appears unlikely that Douglas-fir needle toughness is a mechanism of resistance to the western spruce budworm. Both field observations on mature trees and greenhouse measurements on vegetatively propagated clones failed to produce any evidence that needle toughness was associated with resistance to budworm herbivory (Table 3).

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Burr & Clancy (1993) assessed the possibility that one or more anatomical characteristics of Douglas-fir needles might affect susceptibility to herbivory by the budworm. They compared 23 anatomical characteristics of current-year needles collected from five of the pairs of phenotypically resistant and susceptible trees at the Pike National Forest site. They discovered that needles from resistant trees actually had thinner epidermal layers than needles from susceptible trees (P = 0.038; Table 3). However, they noted that the differences they observed in thickness of the epidermal layer of needles between the putatively resistant and susceptible trees were “probably the result of dissimilar defoliation histories”. Burr & Clancy (1993) suggested that anatomical characteristics of needles might emerge as a mechanism of resistance if vegetatively propagated scions from the resistant and susceptible trees were grown without dissimilar defoliation histories. Chen, Kolb, & Clancy (unpublished data) subsequently evaluated the toughness of current-year needles collected from 12 pairs of cloned Douglas-fir plants derived from resistant and susceptible mature trees (Table 3). Foliage toughness did not differ between the resistant versus susceptible clones 2.5 LOW NUTRITIVE QUALITY OF DOUGLAS-FIR FOLIAGE There is abundant evidence indicating that low nutritive quality of foliage may be an important mechanism of resistance in Douglas-firs against the western spruce

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budworm (Clancy, 1991a, 1992a, 1992b, 2001; Clancy & King, 1993; Clancy et al., 1993). This is somewhat surprising given the tremendous variation in foliar concentrations of primary metabolites (i.e., nitrogen, carbohydrates, and minerals) in trees that is associated with the age of the tree and the leaves or needles, the genotype of the tree, and the environment the tree is growing in (Clancy et al., 1995). Nitrogen (N), or protein, is considered to be the most important nutrient for insect growth and survival (Mattson, 1980; Mattson & Scriber, 1987). However, the importance of N as a key nutrient is probably not strictly cause and effect, but is related to the strong link between N and many other important nutritional factors in plants (Clancy et al., 1995). The western spruce budworm’s response to increased N in artificial diets was neither positively linear nor convex, and it was dependent on levels of minerals in the diets (Clancy, 1992a). Host plant N appears to determine the amount of food the budworm ingests, which in turn affects the amounts of other nutrients consumed; this implies that a proper balance of many different nutrients is probably the most important factor in the nutritional ecology of the budworm (Clancy, 1992a). Indeed, Clancy (2001) reported that the resistant Douglas-fir trees from three different sites consistently had higher levels of foliar N compared to the susceptible trees (P < 0.001; Fig. 2). This result lends further support to the importance of a proper balance of N, minerals, carbohydrates, etc. in determining the quality of foliage as a source of food for budworm larvae. Clearly, higher levels of foliar N do not invariably promote improved budworm survival and reproduction.

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Likewise, Douglas-fir trees resistant to budworm defoliation had higher levels of sugars in their foliage than susceptible trees at all three sites (Clancy, 2001). This is in agreement with results from artificial diet bioassays; budworm fitness was best on artificial diets with sugar (i.e., sucrose) concentrations of 6% dry weight, which is near the lower limit observed for Douglas-fir foliage (Clancy, 1992b) (Fig. 3).

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The budworm’s response curve to different levels of sugar in artificial diets can be used to estimate how budworm populations would grow over three generations if they were feeding on trees that had the average concentration of foliar sugars that occurs in susceptible (10.20 %) versus resistant (11.53%) Douglas-firs (Fig. 3). I simply extended the susceptible and resistant points indicated on the x- (% Sucrose) axis up to the response curve for the appropriate generation (see the y-axis) and projected that point over to the z-axis (No. larvae [log scale]) to estimate the number of first instars alive at the beginning of the and generations. Then, I plotted the projected population growth data to illustrate the comparison for resistant versus susceptible trees. This exercise indicated that budworms feeding on susceptible trees with 10.2% sugars would have 1.4 times greater population growth than budworms feeding on resistant trees with 11.5% sugars (Fig. 4). The differences I have observed between resistant and susceptible trees in concentrations of foliar sugars could have real biological significance in affecting population dynamics of the western spruce budworm.

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Resistant Douglas-fir trees at all three sites also had lower mineral/N ratios in their current-year foliage than susceptible trees for phosphorus (P)/N magnesium (Mg)/N, potassium (K)/N, and zinc (Zn)/N (Clancy, 2001). I repeated the exercise

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described above for sugars using the response curves for ratios of K/N and Mg/N (unpublished data). It was obvious that differences between resistant versus susceptible trees in K/N and Mg/N ratios could also affect budworm population dynamics (Figs. 5 and 6). Budworms feeding on susceptible trees with average K/N ratios of 0.768 were projected to have 2.1 times greater population growth compared to budworms feeding on resistant trees with average K/N ratios of 0.642 (Fig. 5). The predicted effects of variation in Mg/N ratios were even more dramatic. Budworm populations were estimated to increase 8.2 times more when feeding on susceptible trees with average Mg/N ratios of 0.0780 than when feeding on resistant trees with average Mg/N ratios of 0.0661 (Fig. 6). 2.6 DEFENSIVE FOLIAGE

COMPOUNDS

(MONOTERPENES)

IN

DOUGLAS-FIR

Evidence that foliar monoterpenes function as a mechanism of resistance in Douglas-fir to the western spruce budworm is mixed, and thus, controversial (Chen, 2001). Certain monoterpenes (e.g., tricyclene, camphene, and bornyl acetate) have been reported to have adverse effects on budworm performance (Cates et al., 1983; Redak & Cates, 1984; Cates & Zou, 1990; Zou & Cates, 1995). However, the studies that my collaborators and I have conducted do not support an important role for monoterpenes as defensive compounds against the budworm. Clancy et al. (1992) evaluated the effects of terpene compounds on budworm survival and reproduction by forming gelatin-walled microcapsules around eight terpenes that are common constituents of Douglas-fir oleoresin. The microencapsulated terpenes were mixed into artificial diets to determine the effects they had on budworm fitness, using the three generation bioassay technique developed by Clancy (1991b). Five monoterpenes tested ( camphene, myrcene, and limonene) had little or no detectable effect on budworm fitness, when they were tested at concentrations found in Douglas-fir foliage (Clancy et al., 1992; Clancy, 1993; unpublished data). One oxygenated monoterpene, bornyl acetate, had negative effects on budworm fitness at higher concentrations, implying it may function as a defensive chemical (Clancy, 1993). The other two oxygenated monoterpenes assessed (linalool and ) had no detectable effects on budworm fitness at concentrations that occur in host foliage (Clancy, 1993). Furthermore, there were no detectable differences in foliar concentrations of total ( Fig. 7) or individual terpenes between Douglas-fir trees that were resistant versus susceptible to budworm defoliation at any of the three sites (Clancy, 1991a; Clancy et al., 1993; Clancy, 2001). Chen (2001) also failed to find consistent differences in foliar terpenes between resistant and susceptible clones in greenhouse studies. In the 1998 greenhouse bioassay, there were significant differences between the resistant versus susceptible clones. However, the susceptible clones had higher concentrations of monoterpenes in their foliage, which is opposite to what one would expect if terpenes were important in determining

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resistance to budworm defoliation in the field. There were no differences between the resistant and susceptible clones in the concentration or composition of monoterpenes in the 1999 experiment. Collectively, these results suggest that budworm population growth is probably largely unaffected by foliar terpenes.

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2.7 INDUCED DEFENSES IN DOUGLAS-FIR FOLIAGE Chen (2001) addressed the question of whether induced changes in foliar monoterpenes are likely to be involved in resistance of Douglas-fir to the western spruce budworm in the greenhouse bioassays he conducted with resistant and susceptible clones. Two years of defoliation by budworm larvae had similar effects on monoterpene concentrations of clones from resistant and susceptible trees. This result does not support induction of monoterpenes as a mechanism of resistance. 2.8 INDUCED SUSCEPTIBILITY IN DOUGLAS-FIR FOLIAGE Clancy et al. (1993) speculated that the biochemical differences they observed between putatively resistant and susceptible Douglas-fir trees at the Pike and Kaibab National Forest sites could be the result of different budworm defoliation histories. If this is the case, it suggests that budworm defoliation could have a positive feedback for subsequent generations, as in the “resource regulation hypothesis” proposed by Craig et al. (1986). The authors conjectured that “Perhaps the foliar chemistry of susceptible trees is more prone to change in response to defoliation, whereas the resistant trees are less prone to induced changes in chemistry from defoliation. Consequently, susceptible trees may become a better source of food for the larvae with consecutive years of damage, but resistant trees do not become progressively better hosts for the insects. This could explain why budworm outbreaks have persisted for many years in some locations (Brookes et al., 1987).” In addition to addressing the question of induced resistance described in the previous section, Chen (2001) also tackled the issue of induced susceptibility in the greenhouse bioassays he conducted with resistant and susceptible clones. Induced susceptibility could be implicated as a mechanism of resistance if the budworm defoliation treatments had divergent effects on foliar nutrients. (The evidence summarized in the previous two sections leads me to dismiss a potential role for changes in monoterpenes being involved in this mechanism.) The susceptible clones would have to become a better match to the budworm’s nutritional requirements subsequent to being defoliated by budworm larvae, whereas foliar nutrients in the resistant clones should either not change, or change in a direction that made them a poorer match. The statistical analysis of the foliar nutrient data from Chen’s experiments is currently underway, so I cannot yet provide a conclusive answer to this intriguing question. 2.9 DOUGLAS-FIR MICROBIAL MUTUALISTS I do not have any evidence to support a role for microbial mutualists in determining resistance of Douglas-firs to defoliation by the western spruce budworm. However, only preliminary investigations have been conducted to date. Stanley Faeth (Professor at Arizona State University, Tempe) and I collaborated on a pilot study (1996-1997) to examine fungal endophytes in current- year needles

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from the 12 pairs of resistant and susceptible trees at the Kaibab National Forest site. There were no obvious differences in the fungal endophyte fauna of the resistant versus susceptible trees, so we did not pursue this any further (S.H. Faeth & K.M. Clancy, unpublished data). On the other hand, we know that budworm defoliation can influence the ability of Douglas-firs to support ectomycorrhizal mutualists. Kolb et al. (1999) reported that Douglas-fir seedlings that were severely defoliated by western spruce budworm larvae in greenhouse experiments had less ectomycorrhizal colonization than moderately defoliated or non-defoliated trees. Barbara Palermo (M.Sc. student at Northern Arizona University, Flagstaff) recently completed a greenhouse experiment designed to examine the potential role of ectomycorrhizae as Douglas-fir murualists that influence resistance to the western spruce budworm. The data are currently being analyzed, so the results are still pending. Palermo used half-sib seedlings grown from open-pollinated seeds collected from 11 of the 40 pairs of resistant and susceptible Douglas-fir trees (i.e., 22 families) to determine if there are tri-trophic interactions among Douglas-firs, their ectomycorrhizal symbioants, and the western spruce budworm. Experimental treatments included controls, ectomycorrhizal inoculation, or fertilization (with N, P, Mg, and Zn) of resistant and susceptible seedlings. Budworm larval feeding preferences and foliar levels of N, P, Mg, and Zn were measured. Palermo hypothesized that mycorrhizal infection could increase the foliar concentration of key mineral elements (N, P, Mg, and Zn) beyond the optimal levels for the budworm and thus make the trees less suitable (and less preferred) hosts for budworm larvae. The scenario Palermo envisioned is that the genetics of the host tree (resistant versus susceptible to budworm defoliation) influence the rate of ectomycorrhizal colonization of the roots, which in turn helps determine levels of key minerals in the foliage. This results in less budworm herbivory on resistant trees owing to their inherently greater capacity to support ectomycorrhizal mutualists. This would be a very interesting discovery indeed! 3. SUMMARY At least 10 mechanisms are known to be important in resistance of trees to insect defoliators: 1) Phonological asynchrony between host trees and insect herbivores; 2) Host tree tolerance of defoliation, which is linked to host tree vigor; 3) Host tree compensatory photosynthesis and growth in response to defoliation; 4) Toughness of leaves and needles; 5) Low nutritive quality of foliage; 6) Defensive compounds (or allelochemicals) in foliage; 7) Induced defenses in host trees; 8) Induced susceptibility in host trees; 9) Three-trophic-level interactions among the trees, their insect herbivores, and natural enemies of the herbivores (i.e., predators, parasites, pathogens); and 10) Host tree microbial mutualists such as mycorrhizae and fungal endophytes.

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The western spruce budworm and Douglas-fir were used as a model system to investigate nine of these mechanisms. The research employed a combination of laboratory diet bioassays, field observations of mature Douglas-fir trees that were phenotypically resistant versus susceptible to budworm defoliation, and greenhouse bioassays with grafted clones and half-sib seedling progeny derived from the resistant and susceptible trees. The complicated mechanism of three-trophic-level interactions among Douglas-firs, the budworm, and the budworm’s natural enemies has not been explored. Three mechanisms appear to be important determinants of Douglas-fir resistance to the budworm: phenological asynchrony, tolerance and vigor (i.e. growth rates), and low nutritive quality of foliage. On the other hand, the following four mechanisms were excluded: compensatory photosynthesis, toughness of needles, defensive compounds (i.e. monoterpenes) in foliage, and induced defenses (i.e., induction of foliar monoterpenes). The remaining two mechanisms, induced susceptibility and microbial mutualists, are currently under evaluation. Microbial mutualists may or may not be important; results from a pilot study suggested fungal endophytes are not likely to be involved in resistance. However, the jury is still out in regard to the potential influence of ectomycorrhizae in shaping resistance to budworm defoliation. REFERENCES Barbosa, P., & Wagner, M.R. 1989. Introduction to forest and shade tree insects. San Diego: Academic Press, Inc. Brookes, M.H., Campbell, R. W., Colbert, J.J., Mitchell, R.G. & Stark, R.W. (Tech. Coors.). 1987. Western spruce budworm. USDA Forest Service & Cooperative State Research Service Technical Bulletin No. 1694. Burr, K.E., & Clancy, K.M. 1993. Douglas-fir needle anatomy in relation to western spruce budworm (Lepidoptera: Tortricidae) herbivory. Journal of Economic Entomology 86:93-99. Cates, R.G., & Zou, J. 1990. Douglas-fir (Pseudotsuga menziesii) population variation in terpene chemistry and its role in budworm (Choristoneura occidentalisi Freeman) dynamics, In A.D. Watt, S.R. Leather, M.D. Hunter, & N. Kidd (Eds.), Population dynamics of forest insects (pp. 169-182). Andover: Intercept Ltd. Cates, R.G., Redak, R.A., & Henderson, C.B. 1983. Patterns in defensive natural product chemistry: Douglas fir and western spruce budworm, In P. Hedin (Ed.), Plant resistance to insects (pp. 3-19). Washington: American Chemical Society. Chen, Z. 2001. Genetic variation in resistance mechanisms of Douglas-fir to western spruce budworm herbivory. Ph.D. dissertation. Flagstaff: Northern Arizona University. Chen, Z., Kolb, T.E., & Clancy, K.M. 2001. Mechanisms of Douglas-fir resistance to western spruce budworm defoliation: bud burst phenology, photosynthetic compensation and growth rate. Tree Physiology 21:1159-1169. Chen, Z., Kolb, T.E., Clancy, K.M., Hipkins, V.D., & DeWald, L.E. 2001. Allozyme variation in interior Douglas-fir: association with growth and resistance to western spruce budworm herbivory. Canadian Journal of Forest Research 31:1691 -1700. Clancy, K.M. 1991. Douglas-fir nutrients and terpenes as potential factors influencing western spruce budworm defoliation, In Y.N. Baranchikov, W.J. Mattson, F. Hain, & T.L. Payne (Eds.), Forest insect guilds: patterns of interaction with host trees (pp. 124-134). USDA Forest Service General Technical Report NE-153. Clancy, K.M. 1991. Multiple-generation bioassay for investigating western spruce budworm (Lepidoptera: Tortricidae) nutritional ecology. Environmental Entomology 20:1363-1374.

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Clancy, K.M. 1992. Response of western spruce budworm (Lepidoptera: Tortricidae) to increased nitrogen in artificial diets. Environmental Entomology 21:331-344. Clancy, K.M. 1992. The role of sugars in western spruce budworm nutritional ecology. Ecological Entomology 17:189-197. Clancy, K.M. 1993. Are terpenes defensive compounds for the western spruce budworm? Supplement to the Bulletin of the Ecological Society of America 74:193. Clancy, K.M. 2001. Biochemical characteristics of Douglas-fir trees resistant to damage from the western spruce budworm: patterns from three populations, In R.I. Alfaro, K. Day, S. Salom, A. Liebhold, H. Evans, F. Lieutier, M. Wagner, K. Futai, K. Suzuki, and K.S.S. Nair (Eds.), Protection of world forests: advances in research (in press). Vienna: International Union of Forestry Research Organizations Secretariat. Clancy, K.M., & King, R.M. 1993. Defining the western spruce budworm’s nutritional niche with response surface analysis. Ecology 74:442-454. Clancy, K.M., Foust, R.D., Huntsberger, T.G., Whitaker, J.G., & Whitaker, D.M. 1992. Technique for using microencapsulated terpenes in lepidopteran artificial diets. Journal of Chemical Ecology 18:543-560. Clancy, K.M., Itami, J.K., & Huebner, D.P. 1993. Douglas-fir nutrients and terpenes: potential resistance factors to western spruce budworm defoliation. Forest Science 39:78-94. Clancy, K.M., Wagner, M.R., & Reich, P.B. 1995. Ecophysiology and insect herbivory, In W.K. Smith & T.M. Hinckley (Eds.), Ecophysiology of coniferous forests (pp. 125-180). San Diego: Academic Press. Craig, T.P., Price, P.W., & Itami, J.K. 1986. Resource regulation by a stem-galling sawfly on the arroyo willow. Ecology 67:419-425. Dodds, K.A., Clancy, K.M., Leyva, K.J., Greenberg, D., & Price, P.W. 1996. Effects of Douglas-fir foliage age class on western spruce budworm oviposition choice and larval performance. Great Basin Naturalist 56:135-141. Frank, C.J., & Jenkins, M.J. 1986. Impact of the western spruce budworm on buds, developing cones and seeds of Douglas-fir in west-central Idaho, In A. Roques (Ed.), Proceedings conference of cone and seed insect working party (pp. 113-126). Briancon: International Union of Forestry Research Organizations. Gehring, C.A., & Whitham, T.G. 1991. Herbivore-driven mycorrhizal mutualism in insect-susceptible pinyon pine. Nature (London) 353:556-557. Hanover, J.W. 1975. Physiology of tree resistance to insects. Annual Review of Entomology, 20, 75-95. Hardin, J.W., Leopold, D.J., & White, F.M. 2001. Textbook of dendrology. New York: McGraw-Hill. Hermann, R.K., & Lavender, D.P. 1990. Pseudotsuga menziesii (Mirb.) Franco, Douglas-fir, In R.M. Burns & B.H. Honkala (Eds.), Silvics of Northern America (pp. 527). USDA Forest Service Agriculture Handbook No. 654. Kolb, T.E., Dodds, K.A., & Clancy, K.M. 1999. Effect of western spruce budworm defoliation on the physiology and growth of potted Douglas-fir seedlings. Forest Science 45:280-291. Lawrence, R.K., Mattson, W.J., & Haack, R.A. 1997. White spruce and the spruce budworm: defining the phenological window of susceptibility. Canadian Entomologist 129:291-318. Mathiasen, R.L., & Albion, C.S. 2001. Sporocarp production of ectomycorrhiza associated with ponderosa pine in four stand types in Northern Arizona. Harvard Papers in Botany 6:147-154. Mattson, W.J. 1980. Herbivory in relation to plant nitrogen content. Annual Review of Ecology and Systematics 11:119-161. Mattson, W.J., & Scriber , J.M.. 1987. Nutritional ecology of insect folivores of woody plants: nitrogen, water, fiber, and mineral considerations, In F. Slansky, Jr., & J.G. Rodriguez (Eds.), Nutritional ecology of insects, mites, spiders, and related invertebrates (pp. 105-146). New York: Wiley. McMillin, J.D., & Wagner, M.R. 1997. Chronic defoliation impacts sawfly (Hymenoptera: Diprionidae) performance and host plant quality. Oikos 79:357-362. Molina, R., O’Dell, T., Luoma, D., Amaranthus, M., Castellano, M., & Russell, K. 1993. Biology, ecology, and social aspects of wild edible mushrooms in the forests of the Pacific Northwest: a preface to managing commercial harvest. USDA Forest Service General Technical Report, PNWGTR-309. Painter, R.H. 1958. Resistance of plants to insects. Annual Review of Entomology, 3, 267-290.

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Price, P.W. 1991. The plant vigor hypothesis and herbivore attack. Oikos 62:244-251. Price, P.W., Bouton, C.E., Gross, P., McPherson, B.A., Thompson, J.N., & Weis, A.E. 1980. Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annual Review of Ecology and Systematics 11:41-65. Quiring, D.T. 1992. Rapid changes in suitability of white spruce for a specialist herbivore, Zeiraphera canadensis, as a function of leaf age. Canadian Journal of Zoology 70:2132-2138. Redak, R.A., & Cates, R.G. 1984. Douglas-fir (Pseudotsuga menziesii)-spruce budworm (Choristoneura occidentalis) interactions: the effect of nutrition, chemical defenses, tissue phenology, and tree physical parameters on budworm success. Oecologia 62:61-67. Saikkonen, K., & Neuvonen, S. 1993. European pine sawfly and microbial interactions mediated by the host plant, In M. Wagner & K.F. Raffa (Eds.), Sawfly life history adaptations to woody plants (pp. 431-450). San Diego: Academic Press, Inc. Saikkonen, K.S., Faeth, S.H., Helander, M., & Sullivan, T.J. 1998. Fungal endophytes: a continuum of interactions with host plants. Annual Review of Ecology and Systematics 29:319-343. Shepherd, R.F. 1983. A technique to study phenological interactions between Douglas-fir and emerging second instar western spruce budworm, In R.L. Talerico & M. Montgomery (Eds.), Forest defoliatorhost interactions: a comparison between gypsy moth and spruce budworm (pp. 17-20). USDA Forest Service General Technical Report NE-85. Shepherd, R.F. 1992. Relationships between attack rates and survival of western spruce budworm, Choristoneura occidentalis Freeman (Lepidoptera: Tortricidae), and bud development of Douglas-fir, Pseudotsuga menziesii (Mirb.) Franco. Canadian Entomologist 124:347-358. Silen, R.R. 1978. Genetics of Douglas-fir. USDA Forest Service Research Paper, WO-35. Tuomi, J., Niemela, P., Chapin, F.S., III, Bryant, J.P., & Siren, S. 1988. Defensive responses of trees in relation to their carbon/nutrient balance, In W.J. Mattson, J. Levieux, & C. Bernard-Dagan (Eds.), Mechanisms of woody plant defenses against insects: search for pattern (pp. 57-72). New York: Springer-Verlag. Trumble, J.T., Kolodny-Hirsh, D.M., & Ting, I.P. 1993. Plant compensation for arthropod herbivory. Annual Review of Entomology 38:93-119. Wagner, M.R., & Zhang, Z. 1993. Host plant traits associated with resistance of ponderosa pine to the sawfly, Neodiprion fulviceps. Canadian Journal of Forest Research 23:839-845. Zou, J., & Cates, R.G. 1995. Foliage constituents of Douglas-fir (Pseudotsuga menziesii): their seasonal variation and potential role in Douglas-fir resistance and silvicultural management. Journal of Chemical Ecology 21:387-402.

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CHAPTER 4 MECHANISMS OF RESISTANCE IN CONIFERS AGAINST SHOOT INFESTING INSECTS The case of the white pine weevil Pissodes strobi (Peck) (Coleoptera: Curculionidae)

René I. Alfaro 1 , John H. Borden2, John N. King3, Elizabeth S. Tomlin4, Rory L. McIntosh5, Jörg Bohlmann6

1. INTRODUCTION A variety of insects feed on conifer shoots. These include: defoliators, bark, wood and cone borers, girdlers, gall makers and sucking insects, primarily in the orders Lepidoptera, Coleoptera, Hemiptera, Homoptera and Diptera. However, these insects usually do not have an exclusive feeding niche. Some also feed on buds, foliage, stem and cones. For example, larvae of the pine shoot moth, Rhyacionia buoliana Schiff., feed on shoots and cones, in addition to mining inside the newly expanding shoots. Adults of the lodgepole terminal weevil, Pissodes terminalis Hopping, and the white pine weevil, Pissodes strobi Peck, feed on the one-year old or older bark of stem and branches, but the larvae feed exclusively on inner bark of the uppermost tree internodes. As young larvae, spruce budworms, Choristoneura spp., are bud miners, but move to feed on cones and expanding new shoots and foliage as they mature. An important group of shoot infesting insects includes the weevils (Coleoptera: Curculionidae), with the most important genera being Pissodes, Cylindrocopturus and Magdalis. Among these, the white pine weevil is the most important pest of spruce (Picea spp.) and pines (Pinus spp.), in North America (Alfaro 1994; Lavallée and Benoit 1989), and is used in this review as an example to describe defences in conifers to shoot insects. In early spring (late March, April), adults of this weevil emerge from overwintering in the duff, and after mating, females oviposit in the upper section of the previous year's leader. The larvae mine downwards, consuming the phloem, girdling and killing the leader. Pupation occurs in chambers excavated in the xylem. Adults emerge from the leaders from late July to September, and 105 M.R. Wagner et al. (eds.), Mechanisms and Deployment of Resistance in Trees to Insects, 105–130. © 2002 Kluwer Academic Publishers. Printed in the Netherlands.

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when temperatures drop and photoperiod shortens, they go into hibernation in the duff (Silver 1968). Damage from this insect has forced forest managers to eliminate planting of Sitka spruce, Picea sitchensis (Bong.) Carr., in much of the North West Coast of North America (Hall 1994). This insect is now also a threat to white spruce, Picea glauca (Moench) Voss, plantations and with predicted climate change, could expand its range northward above the Arctic Circle (Sieben et al. 1997). Work on genetic resistance to this insect has been pursued in British Columbia (BC), Canada, for the last 30 years, especially at the Pacific Forestry Centre of the Canadian Forest Service, Simon Fraser University, the BC Ministry of Forests, and the University of British Columbia (Alfaro 1996a; Ying 1991;Ying and Ebata 1994). In the last 10 years the BC Ministry of Forests and the Canadian Forest Service initiated a large program to screen Sitka and white spruce for resistance to the white pine weevil. Earlier genetic resistance work was completed in eastern USA, which provided strong evidence for resistance to this weevil on Eastern white pine, Pinus strobus L. (Callaham 1960; Connola 1966; Plank and Gerhold 1965). The resistance-screening program against the white pine weevil in British Columbia is described in the WWW page:

http://www.pfc.forestry.ca/entomology/weevil/resistance/resistance_e.html

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This program consisted of the systematic screening for resistance of over 29,000 individual Sitka and white spruce trees in large, family progeny trials established in replicated sites. Final ranking for resistance was assigned based on field attack rates and laboratory studies. The search for resistant Sitka spruce, which included families collected from Alaska to California, has yielded, so far, only three sources of resistance: Big Qualicum, Haney and the Nass River area (a zone of hybridization between Sitka and white spruce) (Figure 1). Studies in white spruce (also known in BC as interior spruce because of potential hybridisation with Engelmann spruce, P. engelmannii Parry ex Engelm.) have indicated that resistance occurs in the Quesnel Lakes area. Resistance gene pools seem to originate in areas at the edges of spruce distribution, suggesting that resistance is rare and that further efforts to find useful genotypes should concentrate in these areas. This intensive search for spruce with resistance to the white pine weevil gave us the opportunity to conduct research into the mechanisms used by spruces to defend against shoot insects. We found that most defences to this shoot insect also occur in other parts of the tree and are non-specific, i.e. they protect the shoot against a variety of attacking organisms. 1.1 HOST-INSECT INTERACTIONS Conifers use several mechanisms to defend against stem-invading insects (Berryman 1972, 1988; Feeny 1976; Cates and Alexander 1982; Lieutier and Berryman 1988; Mattson et al. 1988; Reid and Watson 1966; Shrimpton 1978). These often occur simultaneously, but the relative importance of each component to successful host defence differs with both host and insect species (Matson and Hain 1985) (Figure 2). Plant defences have been classified according to their permanence in time, into constitutive and induced defences (Berryman 1972,1988; Feeny 1976; Rhoades and Cates 1976, Lunderstadt 1999). Constitutive defences are permanent structural or chemical defence systems that occur regardless of the presence of the attacker. Examples of constitutive defence structures include plant trichomes, thorns, latex and resin canals and an array of chemicals, including resin constituents.

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Inducible defences are activated in response to attack. Examples of inducible defences are the mobilisation of defensive chemicals to the site of wounding, and the production of traumatic resin in conifers in response to insect or fungal attack (Berryman 1988; Raffa 1991; Reid et al. 1967; Reid and Shrimpton 1970; Shrimpton 1978). Guild defences are population strategies used by plants to avoid or confuse herbivores, for example, by virtue of being rare, occurring in mixtures with other species or lacking visual or chemical apparency (Feeny 1976). Another common defensive strategy in plants is preventing damage, for example, by being in the wrong phenological stage at the time of feeding. Plants and insects also evolved forms of multitrophic defence systems in which herbivores induce emission of volatiles from the plant that serve as chemical attractants for predators or parasitoids of the herbivore. Herbivores and plants have co-evolved over the millennia and herbivorous insects have developed many adaptations to mitigate the effects of plant defences on them (Panda and Kush 1995, Alfaro et al. 1999). 2. STUDY OF RESISTANCE MECHANISMS: METHODS The methods used to study resistance of conifers to insects depend on whether the objective is mass screening for accelerated breeding programs or the identification of specific resistance mechanisms. In the case of the white pine weevil, we used field-testing to mass screen the spruce genetic resources of BC, and we (and others) also developed specific tests for particular resistance mechanisms, as indicated below. Field observations of visitation or attack rates on susceptible and resistant trees, and correlations with tree phenology (Hulme 1995; McIntosh 1997; Alfaro et al. 2000b)

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Laboratory behavioral studies employing choice and no-choice experiments (VanderSar 1978; VanderSar and Borden 1977a,b; Alfaro et al. 1979, 1980; Tomlin and Borden 1996) Dissections and life table observations and study of mortality factors (Silver 1968, Therrien 1995). Specific studies to compare structural constitutive defences in resistant and susceptible trees, e.g. measurement of bark thickness, density of bark resin canals, number of sclereid cells (Stroh and Gerhold 1965, Tomlin and Borden 1994a, Alfaro et al. 1997; Grau et al. 2001; O’Neill et al. 2001). Studies to quantitatively and qualitatively measure inducible defences at the molecular genetic, biochemical and chemical level in species and genotypes of spruce, including: wound responses of naturally infested or artificially wounded shoots, histology of wounded leaders and measurement of the strength of traumatic resinosis (Alfaro 1995; Alfaro et al. 1996a; Tomlin et al. 1998; O’Neill et al. 2001); kinetics of traumatic resin production by detecting the expression of terpene synthase enzymes and genes (Martin et al. 2001; Bohlmann unpubl. results; A. Plant, Simon Fraser U., Burnaby, BC, Canada, unpubl. obs.); and chemistry of constitutive and traumatic resin (Martin et al. 2001; Tomlin et al. 2000; Nault and Alfaro 2001) 2.1 FIELD-TESTING FOR RESISTANCE This method involves the planting of candidate genotypes in replicated trials. Genotypes are discriminated as resistant or susceptible by exposure to natural (Alfaro and Ying 1990; Kiss and Yanchuk 1991) or artificial (King and Alfaro 2001) infestations. Releasing weevils in plantations to create artificial infestations is recommended, because screening is faster and more reliable than depending on natural infestations. Artificial infestations are initiated once spruce trees reach attackable height (1-2 meters in height in coastal BC). Results are obtained within one or two years after infestation. This method is cheap and effective; however, it provides only a general ranking of the resistance level, with only limited information on the mechanisms involved. One type of information that we found useful in understanding resistance mechanisms to shoot insects was measuring the rate of Attack Failure among various genotypes. Failed attacks are those cases in which the insect has laid eggs that failed to develop into viable larval populations due to drowning of the eggs and young larvae in toxic resin. Although the shoot survives a failed attack, egg niches and scars due to mining by the larvae are visible. A wide range of resistance to the white pine weevil was revealed by studying rates of oviposition by P. strobi among Sitka spruce clones and ramets from nine

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provenances tested at Fair Harbour, BC (Ying 1991) (Figure 3). In the susceptible provenances (Aberdeen, Fair Harbour, Moresby, Tasu, Muir) virtually every leader with eggs was killed (Figure 3). Clones from provenances with intermediate resistance (Cedarvale, Kitwanga, Green Timbers) sustained high rates of oviposition, suggesting strong attraction, and low feeding and oviposition repellency. However, the leaders were killed at moderate levels, suggesting only mild antibiotic effects, i.e. mild toxicity was exerted on the weevil larvae. Clones from the most resistant provenance (Haney families 0 and 1) had significantly lower oviposition and leader kill rates than the rest, suggesting high levels of repellency (physical or chemical) and toxicity. The most resistant genotype (Haney family 0, clone 2, also known for its registration number as #898), sustained consistently low oviposition rates, with about 12% of the ramets having oviposition at the Fair Harbour trial, of which only about 6% resulted in leader kill.

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2.2 INSECT BEHAVIOR AS INDICATOR OF TREE RESISTANCE Knowledge of host-selection behavior and patterns of dispersal are important to understand plant defences and to develop ecologically durable polygenetic resistance. Studies of visitation rates (or avoidance), disclose within and between plant variations in plant defences. However, such studies require standardization since there is significant variability in circadian and seasonal movement and dispersal behavior (McIntosh et al. 1997). Studies of marked P. strobi (McIntosh 1999) in white spruce showed circadian and seasonal movement within and between trees (Figure 4) (McIntosh et al. 1996;

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McIntosh 1997). Extensive feeding activity occurred in the lower stem and the undersides of lateral branches before weevils moved to the one-year old terminals to feed and lay eggs, suggesting a temporal variation in within-plant resistance. Interestingly, weevils spent a relatively short amount of time at the site of oviposition and brood development, the one-year old leader, preferring to remain on the lower stem and in the foliage of lower order branches particularly during times of the day when temperatures were high (Figure 4). These observations supported the contention that, in addition to localised, within-plant resistance, feeding and oviposition behavior is strongly influenced by environmental conditions (Sullivan 1961). In studying seasonal dispersal patterns of weevils, McIntosh (1997) and (Harman 1975) showed that most movement occurred locally, on average within 3-4 trees (approximately 3-5 m) in a series of small steps. The result is a highly uneven spatial distribution of insects in the plantation, with some susceptible plants escaping attacks and some moderately resistant plants sustaining heavy insect pressure. Therefore, such skewed distributions must be taken into consideration when ascribing resistance ranking to tree genotypes. We concluded that comparative studies to understand within-plant variation in resistance by observing the presence of the insect on the plant must be preceded by a clear understanding of the insect's behavior and preferences.

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2.3 PLANT APPARENCY Barring escape, trees that survive without oviposition under heavy weevil pressure, are either not apparent, i.e. they lack visual or chemical stimuli that cue the insect into the plant, (Feeny 1976), or they contain feeding or oviposition deterrents (Tomlin and Borden 1996). Attributes that are attractant or repellent influence the intensity, distribution and duration of weevil attack in space and time. Apparency increases by having an appropriate leader silhouette (VanderSar and Borden 1977b), or potentially attractive odors (Tomlin et al. 1997). In evaluating genotypes of Sitka spruce (all from resistant provenances) for total amounts of foliar terpenes, we found one genotype with almost twice the amounts as in susceptible trees (Tomlin et al. 1997). Assuming that volatile terpenes are

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involved in host selection, this genotype would be very apparent. Some genotypes had similar levels of foliar terpenes as susceptible control trees, but five had levels that were 20 high-quality clones that do not have some relatedness and therefore a genetic bridge for insect resistance to develop (Libby 1982). Until the early 1990s, clonal diversity had been more apparent than real. For example, although probably several hundred clones have been developed in the U.S., only 3-9 were recommended for nursery production in the Lake States (Hansen et al. 1994). Realizing the potential for plantation disaster, most countries and industries have been working to scale up the number of clones available for deployment. In Ontario, the goal was to have more than 50 clones available at any one time with an annual replacement of 5-10% of the clones recommended for planting as problems arose with older clones and/or much more productive clones became available (Hall 1993). Also, clones being deployed are specifically suited to each soil type and planted in monoclonal blocks no larger than

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5 ha in size. In Oregon and Washington, U.S.A., only one clone from any full-sib family is taken into production (Hall 1993). To date, few experiments have attempted to evaluate the effect of multiple-clone deployment strategies on pest populations and damage levels. Nordman (1998) evaluated three clonal deployment strategies on larval gypsy moth, Lymantria dispar L. (Lepidoptera: Lymantriidae). Two Salix clones were used: SV1 (S. dasyclados, not resistant to L. dispar) and SH3 (S. purpurea, resistant to L. dispar). These clones were arranged in three deployment patterns in the greenhouse: monoclonal blocks, monoclonal mosaics, or clonal rows. Gypsy moth larvae were released in the center of each pattern and allowed to disperse and feed for 10 days. Significant defoliation differences occurred as a result of the clonal deployment pattern. As expected, the least damage occurred on the monoclonal block of the resistant clone SH3. Clonal rows provided better levels of pest resistance than did monoclonal mosaics or the monoclonal block of the non-resistant clone SV1. Presumably, this occurred because larvae spent more time searching for a suitable food source and less time eating. In nature, additional time spent searching for food is detrimental to pests, as their exposure to natural enemies and abiotic hazards is increased. Peacock et al. (1999) demonstrated the spatio-temporal dynamics of a chrysomelid beetle on short-rotation willow in the United Kingdom. Three willow clones (one highly-, one moderately-, and one non-preferred for feeding) were planted as monoclonal blocks or clonal rows. Adult Phratora vulgatissima L. (Coleoptera: Chrysomelidae) were shown to aggregate on the preferred clone in both deployment strategies. However, much more time was needed for the beetles to find the preferred clone when in the clonal row pattern, potentially increasing their exposure to natural enemies as well as delaying development. Another group of strategies related to plantation management includes those borrowed from traditional agricultural systems. These also may work in shortrotation forestry systems. Crop rotation is a common pest management tactic used in agriculture. The same crop or variety is seldom planted in the same field in repeated years, as many pests overwinter in duff or soil within the field or in nearby ground cover or litter. This strategy prevents the pest buildup over several years, as each spring the previous year’s food source is not present, causing them to move on or make use of the new crop. This strategy may work in SRWC systems; however, it is not nearly as applicable. For instance, by the end of a Populus rotation (8-12 years) new clones are available that are superior to the clones previously planted. Perhaps a more appropriate cultural method would be to leave an area fallow for a year before replanting a SRWC system. Chrysomela scripta F. (Coleoptera: Chrysomelidae) are believed to overwinter in leaf litter near their summer food source. By leaving a plantation fallow after harvest, emerging adults would be forced to find a new food source the following spring. Sage et al. (1999) showed that three chrysomelid beetle species overwinter outside Salix biomass plantations and re-infested them each spring. Planting a clonal buffer around the desired clones may be a way to control these pests. The buffer rows could be chemically treated or genetically modified with an insect resistant gene while the interior of the plantation could be left untreated, thus creating an insecticidal border around the plantation. This would reduce or

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eliminate the beetle population that reached the interior untreated area of the plantation. Additional clonal deployment strategies with respect to genetically engineered plants will be discussed in section 2.1.4. 1.3 GENETIC ENGINEERING VERSUS TRADITIONAL TREE BREEDING If the use of host genetics in forest pest management was easily achieved it would probably be more widely used. Research in the use of host genetics to disrupt pest populations has traditionally proceeded through selection and breeding programs. More recently, biotechnology has begun to play an increasingly important role combining the two approaches into a single program (Hart et al. 1992). Genetically modified (GM) trees have the potential to substantially increase wood production in the U.S. (Pullman et al. 1998). From a pest management perspective, genetically engineering toxic genes into trees seems to be an excellent means of pest control. However, changes created by genetic engineering are very different than those brought on by natural evolution or traditional tree breeding and selection. This tactic introduces organisms into the environment that would not otherwise exist there, providing a potential risk to native flora and fauna. Yet, if properly managed, GM trees have the potential to cause little or no damage to the current state of the environment. Several authors have provided excellent reviews on the benefits and risks of GM trees (Raffa 1989, Boulter et al. 1990, McGaughey and Whalon 1992, James 1997, Raffa et al. 1997, James et al. 1998, Jouanin et al. 1998, Pullman et al. 1998). Summarized below are some of the benefits and risks associated with GM trees: Benefits: 1. Pesticide replacement. The use of GM trees in SRWC systems would reduce the amount of pesticides applied to plantations and subsequently lost into the environment via drift, leaching, etc. (Raffa 1989, James 1997). It has been estimated that only 0.1% of the average pesticide application actually reaches the target pest (Pimental 1995). Trees possessing genetic toxicity to insects would eliminate the pesticide lost (an estimated 99.9%) in the environment while simultaneously providing much more efficient insect control. Furthermore, by not investing the time, effort, and physical resources needed for large-scale pesticide applications, great economic savings could be achieved. GM trees also would provide equal pest protection for the entire growing season regardless of weather (Boulter et al. 1990), a luxury rarely attained using chemical sprays, and especially important in managing multivoltine pests. 2. Increased productivity. Trees genetically engineered for pest resistance may not only reduce pesticide cost and input into the environment, but also greatly improve tree productivity by reducing defoliation-related losses. Coyle et al. (2002b) showed the negative effect C. scripta defoliation had on Populus aboveground volume accumulation. Volume was more than 70% greater in chemically

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protected trees compared to controls. Also, fast growing trees contribute more carbon sequestration activity than do slower growing trees. The increased productivity potential associated with transgenic trees could help make SRWC Populus an effective source of wood and wood-based products. 3. Source of the toxic gene. Most GM Populus contain either a Bacillus thuringiensis (Bt) gene or a proteinase inhibitor, both of which are naturallyoccurring and have relatively well-defined target specificity. Furthermore, these genes are biodegradable and usually non-toxic to mammals, birds, and other vertebrates (Boulter et al. 1990). However, because GM trees do not occur naturally in nature, they are not considered true biological control pest management methods even though the pest control tactic they employ occurs naturally. 4. If clonal sublines can be developed with different transgenes for resistance to a particular pest, then plantations could be established as single tree mosaics at the subline resistance level, but as monoclonal blocks from the standpoint of the other commercial traits of a clone (Klopfenstein et al. 1993b). This approach would combine the pest management benefits of single-tree mosaics with the logistical and commercial benefits of monoclonal block plantations. Risks: 1. Biotype evolution. This is defined as the selection for pest populations able to tolerate the new resistance mechanism (Gould 1988). Evolution of new biotypes is the most important risk associated with the deployment of GM plants, and creates an ineffective system in which the GM plant is no longer toxic to the target organism (Raffa 1989, James 1997, Klopfenstein and Hart 1997, Raffa et al. 1997). This is particularly problematic when dealing with trees because of their long life cycle. A single SRWC rotation of 8-12 years can encompass enough insect generations to allow new biotypes to develop (James 1997). Also, the transgene is expressed continually in the plant, thus constantly exposing insects to the toxin, a process that accelerates resistance. Bauer (1995) reported on 13 species (including C. scripta) that have already developed resistance to Bt in the laboratory. 2. Effects on non-target organisms. The potential for GM plants to adversely affect non-target organisms is of great concern. Perhaps the most well-known and controversial example is the recent finding that corn pollen containing a Bt toxin has the potential to negatively affect monarch butterfly, Danaus plexippus L., (Lepidoptera: Danaidae) larval survival and development (Losey et al. 1999, Hansen-Jesse and Obrycki 2000). These studies have initiated an intense controversy and increased the number of studies into the non-target effects of transgenic plants. Other studies also have found Bt toxins to negatively affect beneficial organisms (James et al. 1993). There also is a risk of predatory insects acquiring toxins through the consumption of contaminated prey. Reducing predator populations this way would not benefit transgenically gained protection, as predator complexes often compliment transgene pest control. Overall, much less research has been conducted on the effects of GM trees on non-target organisms.

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3. Transgene escape. Substantial environmental damage could occur if the transgene increases the fitness of the host tree under wild conditions (Raffa 1989, James 1997, Raffa et al. 1997, DiFazio et al. 1999). The longevity of the escaped GM tree may be greater than that of the original non-GM tree, resulting in increased probability that GM trees could establish in the wild or interbreed with non-GM trees. Hypothetically, GM trees could be more invasive than non-GM trees, thus outcompeting native host trees for available resources. This also could happen if GM trees exhibited an increased growth rate, reaching reproductive maturity earlier than non-GM trees. One way to combat this might be to genetically engineer reproductive sterility. The research group led by Dr. S. H. Strauss at Oregon State University is working on this issue, and has inserted some transgenes that may give sterility (Strauss et al. 1995). This could solve many of the risks associated with the deployment of GM trees. Adequate risk assessment of GM Populus is necessary if these plants are to be used in SRWC systems safely and effectively (Raffa et al. 1997). Relying on the pest resistance of the transgenic plant alone will almost certainly result in increased biotype formation, thus negating the insecticidal effects of the transgene. Supplemental pest control with pesticide applications, utilizing clonal deployment strategies, and GM crop rotation are effective ways for managing insect resistance. 2. REVIEW OF HOST PLANT RESISTANCE IN POPULUS AND SRWC SYSTEMS 2.1 RESISTANCE TO CHRYSOMELID BEETLES 2.1.1 Clonal variation Developing and selecting insect and disease resistant clones should be emphasized as the primary defensive strategy against pests in short-rotation Populus. A great deal of information has already been learned about this group of pests. Chrysomela scripta is the most important defoliator of Populus in the eastern U.S. (Burkot and Benjamin 1979). Both adults and larvae of this multivoltine insect can severely damage branch terminals, and its ability to rapidly increase populations can lead to widespread economic damage in young plantation Populus (Harrell et al. 1981, Coyle et al. 2002b). While synthetic (Abrahamson et al. 1977) and biorational (Coyle et al. 2000) chemical controls have proven effective in controlling C. scripta in plantation Populus, these methods are neither environmentally-friendly nor provide a long-term solution to the pest management problem, respectively. Through the process of selective tree breeding, favorable traits can be combined in superior tree cultivars. This process is ongoing and new clones are continually being developed. Because of the large number of clones potentially available for large-scale clonal deployment, careful screening must be completed to ensure that only clones with positive attributes are chosen. Several general principles have been

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established regarding C. scripta as a result of clonal screening trials, particularly in the areas of oviposition and feeding preference as well as performance. Caldbeck et al. (1978) examined C. scripta feeding preference on 33 Populus clones. Both adult and larval C. scripta defoliated trees. Visual damage estimates were used to assess beetle preferences. Clonal preferences were observed, and followed lines of sectional parentage. Clones in the section Populus ( = Leuce) (e.g. containing P. alba parentage) showed minimal damage, whereas clones in the Aigeiros (e.g. P. deltoides) and Tacamahaca (e.g. P. trichocarpa) sections had a 22 to 78% reduction in leaf area. Haugen (1985) evaluated adult C. scripta feeding and oviposition preference on 12 Populus clones. A multiple choice greenhouse experiment confirmed that adult C. scripta did not prefer Populus section clones for oviposition. Pure species clones in the sections Aigeiros and Tacamahaca were both highly preferred for oviposition, and there was a relationship between Aigeiros parentage and oviposition preference. Clones with a greater amount of Aigeiros parentage were more preferred for C. scripta oviposition than those with greater Tacamahaca parentage. A study by Bingaman and Hart (1992) showed C. scripta’s preference to oviposit on section Aigeiros clones compared to section Tacamahaca clones. Six clones were examined in this study, and two of the top three highest oviposition rates were on clones with section Aigeiros parentage; a section Tacamahaca hybrid was used the least for oviposition. These findings contrast somewhat with those of Haugen (1985), as he found the same section Tacamahaca clone preferred for C. scripta oviposition. Furthermore, oviposition was preferred on pure species in sections Aigeiros and Tacamahaca over intersectional hybrids (Bingaman and Hart 1992). Adult C. scripta feeding preference also was examined in this study. Increased adult C. scripta feeding occurred on clones with a greater percentage of section Aigeiros parentage when compared to clones with section Tacamahaca parentage. However, increased adult feeding was shown on clones in the Aigeiros and Tacamahaca sections when compared in multiple-choice bioassays. A P. deltoides P. nigra clone was the most preferred in adult feeding trials; this agreed with Caldbeck et al. (1978). Bingaman and Hart (1992) suggested that oviposition preferences followed feeding preferences because adult C. scripta spent more time on these clones, thus having a greater opportunity for oviposition. Previous research showed that C. scripta adult feeding preferences did not correspond with larval performance on Salix host plants (Orians et al. 1997). A study was conducted to determine if adult C. scripta preferentially oviposit on clones that increase larval performance. Larval C. scripta performance was examined on eight Populus clones by measuring larval mortality, pupal weight, adult emergence, and total mortality (Coyle et al. 2001). Larvae generally performed better on section Aigeiros Tacamahaca hybrids as opposed to pure P. deltoides or P. trichocarpa clones. However, environmental factors may play a more important factor in larval C. scripta performance than originally thought, as a seasonal decline in larval performance was evident. Species in the section Populus are not preferred for feeding or oviposition, whether they are pure species or hybrids. Aspens are not natural host plants for C. scripta (Baker 1972), and this antixenotic relationship might be exploited by using

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selections from the Populus section in mixed planting designs. However, section Populus clones are quite difficult to cross with clones in other sections, and it is not clear that anything could efficiently come out of a hybridization strategy. 2.1.2 Foliar chemistry Phytophagous insects usually consider combinations of olfactory, visual, and physical factors when selecting a host plant. Chemical interactions seem to be quite influential in C. scripta host plant selection. Trees in the genus Populus have a suite of secondary compounds throughout their tissues; most notable are the phenolic glycosides (Palo 1984, Picard et al. 1994b, Lindroth and Hwang 1996a). Aspens (P. tremuloides) have at least four phenolic glycosides present in their leaf tissues (salicin, salicortin, tremuloidin, and tremulacin), whereas P. deltoides seems to lack tremulacin (Lindroth et al. 1987). Extensive research on aspen phenolic glycosides has come, from Dr. R. L. Lindroth and his research group at the University of Wisconsin. Lindroth and Hwang (1996b) have written a comprehensive review of this subject. Seasonal fluctuations in the amounts of phenolic glycosides and nitrogen content occur in several Populus species and clones (Dickson and Larson 1976, Lindroth et al. 1987, Osier et al. 2000b). Generally, these chemicals decline over the course of a growing season. However, younger leaves had significantly higher concentrations of phenolic glycosides than did older leaves (Lindroth et al. 1987). Seasonal decline also was found in leaf surface long-chain alcohol and alpha-tocopherylquinone concentrations (Coyle 2000). Herbivory by chrysomelid beetles also influenced Populus foliar chemistry. Populus tremula P. tremuloides clones showed an increase in phenolic glycoside production in response to C. scripta defoliation (Picard et al. 1994a). This resulted in decreased herbivory by the beetle. Bingaman and Hart (1993) examined this relationship with C. scripta and hybrid Populus. Phenolic glycoside (salicin, salicortin, and tremulacin) content was measured on seven hybrid Populus clones. Chemical amounts varied among clone and leaf age class (younger leaves had higher phenolic glycoside concentrations). Tremulacin amounts in hybrid Populus were negatively correlated with C. scripta feeding and oviposition preferences, whereas salicin and salicortin amounts were not. Matsuda and Matsuo (1985) showed that some phenolic glycosides in Salix gracilistyla leaves act as chrysomelid beetle feeding stimulants. Long-chain alcohols on the leaf surface also can serve as phagostimulants to chrysomelid beetles (Adati and Matsuda 1993). Recently, Lin et al. (1998a) discovered a suite of Populus leaf surface chemicals that act as adult C. scripta phagostimulants. Longchain alcohols and were isolated from the P. deltoides P. nigra clone ‘Eugenei’. Artificial leaf disc bioassays were used to examine the effects of these chemicals on adult C. scripta feeding. Alcohols or alone did not stimulate intense feeding behavior, but when used in specific ratios these chemicals induced C. scripta to bite. A subsequent study (Lin et al. 1998b) investigated the interactions between Populus leaf surface phagostimulants from field-grown trees and adult C. scripta. Adult C. scripta feeding preferences were examined for 91

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Populus clones from a University of Washington pedigree line. Feeding preferences were then correlated to the aforementioned phagostimulants and to the phenolic glycosides tremulacin and salicortin. Leaf surface chemical amounts of long-chain alcohols and the phenolic glycosides did not explain C. scripta feeding preferences. However, feeding preference was linked to content. Leaf area consumption increased as concentrations reached , but feeding decreased when levels increased further. This study linked the content on the Populus leaf surface to adult C. scripta feeding preference. It is unknown if Populus trees are able to alter their leaf surface phagostimulant concentrations in response to C. scripta feeding. A study was conducted to examine the effects of larval C. scripta defoliation on the leaf surface phagostimulant concentrations of eight Populus clones. Coyle (2000) found that amounts of these chemicals were not significantly altered by larval C. scripta defoliation. Larval performance did not correlate with leaf surface phagostimulant concentrations; however, both larval performance and leaf surface chemical amounts declined over the course of a growing season. There are many implications and applications from this research. Adult C. scripta Populus clonal preference is mediated by amounts on the leaf surface; however, it is unknown if Populus clones preferred by adult C. scripta for feeding and oviposition are more suitable for larval growth and development. If this proves true, clones less preferred by adult C. scripta could be used in Populus breeding and clonal selection programs. This could, theoretically, produce clones less suitable for larval C. scripta growth and development. Also, the identification of C. scripta phagostimulants can be used in many ways. Efforts have been made to develop an artificial diet for C. scripta (Bauer 1990) as maintaining a laboratory colony is labor intensive and requires much greenhouse space for food trees. The diet developed by Bauer (1990) was nutritionally adequate, but resulted in decreased colony health. Attempts to incorporate Populus leaf surface phagostimulants into the diet to increase C. scripta consumption have been unsuccessful (Coyle and Hart, unpublished data). 2.1.3 Proteinase inhibitor genes Genetic engineering of woody plants is a relatively new technology. Currently, the primary focus is on incorporating genes for pest resistance (Heuchelin et al. 1997, Klopfenstein and Hart 1997). Populus trees are easily manipulated through various genetic engineering methods (Klopfenstein et al. 1997b). Effective procedures have been developed for vegetative propagation of Populus (Faltonson et al. 1983). The ability to genetically manipulate a rapidly growing woody plant with the possibility of quickly increasing plant numbers opens doors to new pest management strategies. Scientists at Iowa State University successfully transformed a hybrid poplar clone, P. alba P. grandidentata, with a wound-inducible proteinase inhibitor II (pin2) gene from a potato (Klopfenstein et al. 1991). Field data showed that transgenic plants did not statistically differ in height or diameter compared to non-transformed controls (Klopfenstein et al. 1993a). This study showed that pest resistance genes can be incorporated into Populus clones without compromising growth.

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Several studies have shown successful incorporation and application of the pin2 gene in hybrid poplar. Reduced leaf area consumption and growth rates occurred when larval Plagiodera versicolora Laicharting (Coleoptera: Chrysomelidae) were fed Populus leaves from clones transformed with the pin2 gene (Klopfenstein et al. 1994, 1997a). Kang et al. (1997) examined transgenic Populus resistance to C. scripta on tissue-culture plantlets of the Belgian clone Ogy (P. deltoides P. nigra) and three sublines transformed with the pin2 gene. Leaf area consumption was reduced by as much as 45% and larval C. scripta weight was up to 16% less on the transformed lines compared with Ogy. Chrysomela scripta resistance on these clones was evaluated in a greenhouse experiment (Coyle et al. 2002a) to determine if the resistance exhibited in plantlets was maintained in young trees. Leaf area consumption and larval C. scripta growth and development were not affected by the presence of the pin2 gene. We can provide several explanations for these results, with environmental differences posing as the main concern when comparing these two studies. Kang et al. (1997) placed larvae in test tubes with the plantlets, whereas Coyle et al. (2002a) conducted their study in the greenhouse. There are many differences between these two environments, including sterility, air composition, and their effects on plant tissue growth. Large increases in plant size accompany the laboratory – greenhouse – field study experimental sequence; this may have had an effect on the efficacy of the pin2 gene. It is not known if a field study would produce results similar to either of the previous studies. European scientists also have had success incorporating proteinase inhibitor genes into Populus for chrysomelid resistance. Leple et al. (1995) showed high levels of gene expression in P. tremulae P. tremuloides clones transformed with a proteinase inhibitor. Transformed clones were toxic to Chrysomela tremulae F. larvae, an important pest of poplars in Europe. This was the first study to successfully transform Populus with a proteinase inhibitor and demonstrate toxicity to chrysomelid larvae. Recently, a proteinase inhibitor gene was incorporated into P. alba (Delledonne et al. 2001) and high levels of resistance to Chrysomela populi L. were obtained. While this technology seems promising, there are still several cases of plants transformed with proteinase inhibitor genes not showing resistance to insect herbivores (Confalonieri et al. 1998, Girard et al. 1998, Coyle et al. 2002a). Insects do possess the ability to adapt to proteinase inhibitor genes just as any other transgenic control method (Jongsma and Bolter 1997). 2.1.4 Transgenic Bt trees Technology has advanced to the point that select Bt toxin genes can be inserted directly into plants for insect control. This pest management tactic is not new to traditional agricultural crops; Bt corn has been commercially sold and field planted since 1995 (Carozzi and Koziel 1997). Currently, cultivars of soybean, cotton, potato, and a host of other crop species have been developed and are registered for use.

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The use of transgenic Bt-expressing plants in forestry systems is still a novel approach to pest management. While the application of Bt formulations to plantation Populus is an effective way to combat pests (Coyle et al. 2000), the use of transgenic trees can be more favorable for a number of reasons (Meilan et al. 2000). Spray drift is reduced, as the Bt toxin is produced in the plant tissues, and the toxin will not degrade as will a sprayed formulation. Also, Bt plants only expose the toxic gene to insects feeding on the plant. Bt toxins differ from proteinase inhibitors in that Bt generally causes direct mortality of the target pest. Proteinase inhibitors have a more subtle mode of action, reducing fecundity, extending the life cycle, and causing reduced weight and changes in insect behavior (Ryan 1981, 1990). Populus was the first woody plant species to be transformed with the Bt gene (McCown et al. 1991). Researchers at Oregon State University have since produced over 1,700 transgenic Populus lines (Strauss et al. 1998). Resistance to C. scripta was evaluated on 51 lines of Bt Populus transformed with an Agrobacterium tumefaciens vector (Meilan et al. 2000). Every transformed strain evaluated showed significantly reduced defoliation and increased growth at the end of one growing season. Robison et al. (1994) and Wang et al. (1996) observed insecticidal effects in poplars with a lepidopteran-specific Bt gene. Large-scale field trials are currently being initiated by Meilan et al. (2000) in the Pacific Northwest and by Wang et al. (1996) in China.

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Reviews by Tabashnik (1994) and Gould (1998) provide excellent summaries of insect resistance management with respect to transgenic crops. These reviews emphasise several resistance management tactics, including mixtures of toxins, refugia strategy, high dose strategy, synergists, and spatial and temporal expression of toxins. The refuge strategy may be the best way to slow the development of insect resistance in transgenic crops (Tabashnik 1994). This strategy employs a refuge of non-transgenic plants planted with transgenic ones. Non-resistant pests are allowed to reproduce without receiving sublethal doses of the toxin, and subsequently breed with resistant pests. This diffuses the gene for insect resistance, thus delaying the species’ or population’s development of resistance. Gould (1998) focuses on the high dose/refuge approach for management of insect resistance to Bt crops (Figure 2). This differs only in that the transgenic plants present with the refuge carry a level of toxicity much greater than needed to kill the pest. If the level is sufficiently high enough, even resistant individuals will be killed by the toxin, and will not be able to pass the resistant gene to future generations. While refuges can be within or adjacent to transgenic plots, adjacent refuges have been shown to be more effective in some systems (Tang et al. 2001). 2.2 RESISTANCE TO OTHER DAMAGING AGENTS There is considerable interclonal variation in secondary chemical amounts present in Populus foliage (Lindroth and Hwang 1996a, 1996b, Hwang and Lindroth 1997, Lin et al. 1998b, Osier et al. 2000b). Insect survival, larval stadium duration, and body weight varied greatly for two larval lepidopterans, L. dispar and Malacasoma disstria Hübner (Lepidoptera: Lasiocampidae), when reared on 13 different aspen clones (Hwang and Lindroth 1997). These differences were more pronounced in L. dispar, where larval survival ranged from 0 to 100% in fourth instar larvae. Fourth instar M. disstria survival ranged from 60 to 100% on the same clones. Lymantria dispar performance was reduced when higher phenolic glycoside concentrations were present in P. tremuloides foliage (Osier et al. 2000a). However, foliar consumption was positively correlated with tannin concentration. Atmospheric and light intensity also may influence larval performance and foliar chemistry. Increased and light levels induced increases in aspen foliar phenolic glycoside content (Lindroth and Kinney 1998, Roth et al. 1998, McDonald et al. 1999). Furthermore, L. dispar larvae had reduced growth rates when fed aspen leaves exposed to increased levels (Lindroth and Kinney 1998, McDonald et al. 1999). Overall, these larval performance reductions were not great, and were not apparent in one study using M. disstria (Roth et al. 1998). Many studies have shown that insect defoliation can induce chemical changes in foliage. Often these are specific damage-induced chemical changes that provide the plant protection (Lindroth and Hwang 1996b). Aspen trees have a well-documented wound-induced chemical protection system. For instance, defoliation by Choristoneura conflictana (Walker) (Lepidoptra: Tortricidae) induces increases in phenolic glycoside content (Clausen et al. 1989). These chemicals are toxic to C. conflictana, and result in reduced larval performance. Larval L. dispar and M. disstria defoliation induced increases in aspen phenolic glycoside content (Lindroth

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and Kinney 1998, Roth et al. 1998). However, only L. dispar performance was correlated negatively with phenolic glycoside content in aspen. Therefore, woundinduced increases in foliar phenolic glycosides are an effective but species-specific natural defense mechanism. Several additional insect pests, including root and shoot borers, sawflies, lepidopterans, and leaf miners, attack Populus plantations (Solomon and Abrahamson 1972, Thomas and Rose 1979, Wilson 1979, Solomon 1988, Sage and Tucker 1997). However, their populations generally do not reach the economically damaging levels of C. scripta, M. disstria, or L. dispar. However, the cottonwood twig borer, Gypsonoma hiambachiana (Kearfott) (Lepidoptera: Tortricidae), can have an economic impact on SRWC systems. Morris (1967) identified this insect as a potentially damaging pest of plantation Populus. High populations have been shown to cause nearly 100% terminal shoot mortality (Stewart and Payne 1975). Current controls include synthetic chemicals (Morris 1960, Coster et al. 1972) and possibly natural biological controls (Morris 1967). Two studies have evaluated P. deltoides clonal resistance to G. hiambachiana (Woessner and Payne 1971, Payne et al. 1972). Pure P. deltoides clones in both studies were more heavily attacked than a hybrid clone. These results imply that Populus hybridization may be required in order to attain resistance to G. hiambachiana, a phenomenon observed in other herbivory studies and reviewed by Fritz et al. (1999). However, McMillin et al. (unpublished data) found varying damage levels among four hybrid Populus clones and across three locations in Iowa (Figure 3), indicating that not all hybrid poplars are resistant to G. hiambachiana damage.

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Recently, McMillin et al. (1998) suggested that increasing the number of actively-growing Populus terminals in a plantation can result in G. hiambachiana population increases. Hence, alternate controls must be attained for this pest, as plantation size will most likely increase as short-rotation forestry gains acceptance and industrial implementation. Disease also is a major issue in short-rotation Populus plantations, and the resulting damage can be equal to or greater than that caused by insects, particularly in the establishment years (Ostry and McNabb 1985). Disease can be managed much the same as insect pests by incorporating host-plant resistance mechanisms and utilizing proper plantation planting and management strategies. Many diseases can damage Populus (Berbee 1964, Shea 1971, Ostry and McNabb 1985, Newcombe 1996). However, only a few are of great economic significance. Melampsora medusae Thuem. (Uredinales: Melampsoraceae) leaf rust is one of the most damaging and widely studied diseases of Populus in North America (Newcombe 1996). This disease can result in premature leaf abscission, reduced growth, increased lateral branching, and early mortality (Newcombe and Chastagner 1993, Newcombe et al. 1996, Callan 1998). Previous studies have shown wide variation in Populus resistance to Melampsora rust (Ostry and McNabb 1985, Newcombe et al. 1994). However, it is becoming clear that selection for complete resistance and the deployment of resistant clones has led to the development of many new rust biotypes that may overcome host resistance. Septoria musiva Peck (Dothideales: Sphaerioidaceae) leaf spot and stem canker is an important cosmopolitan disease of Populus. This fungus generally occurs as leaf spot on native Populus with cankers predominately reported on clones containing Tacamahaca parentage (Bier 1939, Waterman 1946). Stem breakage often occurs well before harvest age, and susceptible clones are generally not utilized in plantations (Ostry et al. 1989). Selecting Populus clones resistant to Septoria through clonal screening is the only way to combat this pest. Clones with Tacamahaca parentage have been shown to be more susceptible than clones with Aigeiros parentage (Ostry and Berguson 1993). This study also showed that selecting canker resistant clones can result in reduced biomass accumulation. However, recent clone selection work with pure P. deltoides germplasm indicates that high yields can be combined with Septoria canker resistance (Hall, unpublished data). Increased growth is often sought by hybridizing Populus rather than planting a single species (Stettler et al. 1996). However, hybridization may sacrifice any natural disease resistance occurring in native species (Fritz et al. 1999). Presently, the only effective way to combat pathogens is by utilizing host plant resistance mechanisms in breeding and selecting resistant clones (Callan 1998). Genes conferring resistance to Melampsora have been discovered in hybrid and pure species Populus (Newcombe et al. 1996, Tabor et al. 2000). Selective breeding and/or genetic engineering may facilitate the incorporation of these genes into new Populus clones. Exapted resistance (that conferred by a non-native species) may play a much larger role in future Populus plantation management (Newcombe 1998). This type of resistance will need to be used in concurrence with other

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resistance mechanisms to effectively combat many of the pathogens occurring on Populus. 2.3 MULTIPLE PEST SCREENING All woody crop species have a varied complex of organisms that have the ability to limit the economic viability of these systems. For example, Populus has at least 24 insect defoliators as well as several pathogens in North America (Dickmann and Stuart 1983). Further complicating the development of deployment strategies for Populus resistance is the fact that different insect species seem to prefer different clones; a resistant clone to one insect is susceptible to a complex of other insects. Thus, screening of advanced clones or selections must include tests across a variety of taxa. Several studies have screened clones for resistance and/or susceptibility to two or more defoliating insects and pathogens. Researchers at the University of Wisconsin screened three Populus clones to C. scripta and M. disstria (Raffa et al. 1991, Ramachandran 1993). Two clones were highly susceptible to C. scripta, but resistant to M. disstria, whereas the opposite was true in the third clone. This tradeoff was caused by the high phenolic glycoside content in M. disstria resistant clones, which positively influences C. scripta, and the low concentration in the M. disstria susceptible clone. This research suggests that the M. disstria resistant clone could be engineered with the coleopteran-toxic Bt gene to create resistance across two taxa (Raffa et al. 1991, Ramachandran 1993). Nordman (1998) screened 19 Salix and six Populus clones for resistance to seven defoliating insects. Two primary results were obtained: a wide range of susceptibility occurred among clones to a particular defoliator, as well as in individual clones to all seven defoliators. Clones resistant to one species often were not resistant to others. This study demonstrates the need for multiple pest resistance screening when preparing clones for commercial use. 3. DEVELOPMENT OF AN IPM PLAN FOR C. SCRIPTA The majority of SRWC commercial hardwood operations have been developed in the Pacific Northwest region of the U.S. and in Europe, but more recently are being established throughout several other locations in the U.S. and Canada (van Oosten 2000). Present management methods for insect pests, such as C. scripta, in commercial plantations are currently quite dependent upon applications of broadspectrum organic or biorational insecticides. Often, this is still done on a calendar schedule, but commercial growers are beginning to recognize the desirability of monitoring for pest activity and levels and timing applications to increase efficacy and reduce losses. They are becoming aware that repeated applications of a single pesticide may contribute to the development of insect resistance to that material. The development and initiation of an IPM program is the next step in Populus pest management. IPM is designed to be more environmentally-friendly and incorporate many different control measures into a pest management strategy. IPM also may help reduce the development of insect biotypes and thus prolong the effective

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commercial life of desirable clones. With some expansion and fine tuning of the existing base of knowledge, we seem to be poised to develop and implement an IPM plan for plantation Populus, particularly for managing C. scripta. Plantations should contain resistant clones, as this will serve as the foundation for C. scripta control. By selecting clones that are less preferred for adult feeding and oviposition we can reduce the amount of time adult beetles spend on the clones, therefore, reducing their tendency to oviposit (Bingaman and Hart 1992). Also, clones that cause poor larval performance and delayed development can be planted to reduce the number of adults present. As stated earlier, multiple lines of resistance are needed to prevent biotype evolution. However, the number of lines needed is still under debate. Unless clones can be developed that are completely resistant to C. scripta, other pest management strategies will also need to be utilized. Biorational sprays are a chemical control method capable of providing excellent C. scripta control. Unlike their synthetic chemical counterparts, biorational sprays containing Bt are environmentally-friendly and non-toxic to vertebrates and most non-target organisms (Tabashnik 1994). Several studies have shown Bt toxins to be extremely effective in controlling C. scripta populations in the laboratory (Bauer 1990, James et al. 1999). Coyle et al. (2000) achieved excellent C. scripta control in the laboratory using two commercially available Bt formulations. These formulations were then applied to a Populus plantation and similar results were attained. Results from Coyle et al. (2000) agreed with previous laboratory studies (Bauer 1990, James et al. 1999) in that susceptibility to Bt was negatively correlated with beetle age and size. Adult C. scripta are far less susceptible to Bt than are larvae, especially the first two instars. Hence, the timing of Bt application is of great importance. Bt formulations will achieve the greatest level of control early in the C. scripta generation, and should be applied when eggs and first instars are the predominant life stages. Coyle et al. (2000) made their applications when there were equal numbers of unhatched and freshly hatched egg masses. After three seasons, Populus trees protected by Bt sprays had produced between 50 and 73% more above-ground volume than their unprotected counterparts (Coyle et al. 2002b). Because the early life stages are the most vulnerable, population monitoring is an essential aspect of C. scripta management. Coyle et al. (2000) visually determined C. scripta life stages; however, this was time consuming and required experienced personnel able to recognize the various life stages. Nebeker et al. (2001) used boll weevil traps to monitor adult C. scripta field populations. Traps provided information on population levels and the current life stage in the field. This information could be used in conjunction with biorational sprays. C. scripta emergence was easily detectable, as extremely large numbers were caught within 12 days. After emergence, adult C. scripta undergo a 5-7 day feeding period during which they become sexually mature (Burkot and Benjamin 1979). Traps can indicate when each beetle generation emerges, and plantation managers can use this information, along with the knowledge of the maturation feeding period, to best predict the most optimal time to apply treatment. Degree-day (DD) calculations also can be used to predict appropriate spraying times. Burkot and Benjamin (1979) found that C. scripta generations required between 222 and 273 DD depending on the generation and temperature. Similarly,

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Jarrard (1997) examined the DD requirements on C. scripta in Iowa. This study observed requirements of between 229 and 317 DD per generation. Jarrard (1997) also found that observed DD requirements were very similar (all within 35 DD) to model-based predicted values. Two studies examined C. scripta DD requirements in Mississippi, USA. Pope and Nebeker (2002) and Nebeker et al. (2001) required 281 DD and 280 DD, respectively, for one C. scripta generation. Their results agreed closely with those of Jarrard (1997). This information is of significant importance. Because DD models seem to be adequate predictors of C. scripta life stages, we can estimate when each C. scripta generation will occur in the field and treat accordingly. Jarrard (1997) found that predicted DD requirements were within two calendar days of development observed in the field. This information can be used to create a better spray schedule based on insect life stage rather than on a strict calendar schedule. This will save not only time and money, but will reduce insecticide applications to plantation Populus. Insecticide applications can be reduced further by incorporating an accurate economic injury level (EIL) (Pedigo et al. 1986) for C. scripta on plantation Populus. Fang and Hart (2000) examined the relationship between larval C. scripta population levels and subsequent plant damage. This study also showed that egg mass densities may be a useful indicator of potential defoliation. A concurrent study by Fang (1997) integrated several factors and derived an EIL for C. scripta of 0.2 – 0.9 egg masses per terminal for the second generation. Populations below this level were not predicted to cause sufficient economic loss to justify pesticide application. Economic gain would occur only when populations or damage above the EIL were treated. Natural enemies do contribute to C. scripta population control, but seemingly not to a great extent in commercial plantations. Burkot and Benjamin (1979) examined the natural enemies responsible for C. scripta mortality in Wisconsin. Natural enemies had the least effect on C. scripta populations during the first C. scripta generation, yet exhibited greater control in successive generations. This was primarily accomplished by coccinellid predation on egg masses and pupal parasitism by a parasitic wasp, Schizonatus latus Walker (Hymenoptera: Pteromalidae). Schizonatus latus parasitized over 25% of the pupae during the third C. scripta generation, and coccinellids accounted for up to 25% of egg mortality in the fourth generation. Jarrard (1997) examined the natural enemy complex in central Iowa. Similar to the study in Wisconsin, coccinellid predators were the most numerous C. scripta natural enemy. The greatest natural enemy influence occurred on egg masses in the second C. scripta generation, where over 70% mortality was recorded. Thus, natural enemies do exert control on C. scripta populations, primarily in the sessile (egg and pupal) stages. However, because of the multivoltine lifestyle and reproductive potential of C. scripta (Coyle et al. 1999) natural enemies alone do not seem to be able to control populations effectively in plantations. In summary, many components of an IPM program for C. scripta have been developed. What is needed is the integration of all the pieces of the puzzle together in different planting strategies for at least one rotation. This could serve not only to test the accuracy of the information elucidated to date, but would serve as a benchmark to determine the most effective directions for additional research.

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4. CLONAL DEVELOPMENT AND DEPLOYMENT STRATEGIES FOR TODAY AND FUTURE RESEARCH NEEDS Based on our experience to date, the best clonal development strategy appears to be to breed and select for tolerance and/or resistance to Septoria and Melampsora diseases and then genetically transform the best clones with the Bt genes or proteinase inhibitors and other insect resistance mechanisms. The mosaics of monoclonal stands deployment strategy seems to have the most potential for large-scale use at this time (Zsuffa et al. 1993), while the high dose/refugia strategy should be added as soon as the problems with commercial plantings of transgenic clones are satisfactorily addressed. Matching clones to specific soil conditions or production objectives will increase the efficacy of these systems further. An obvious, but sometimes overlooked, issue is that clonal deployment strategies can not overcome poor quality clones if they are used in plantings (Zsuffa et al. 1993). To ensure clonal diversity and therefore protect clone longevity and plantation success, Hall (1993) recommends the following: 1) establish a maximum block size that can be planted to one clone, 2) prohibit two fields of the same clone from bordering one another, and 3) within any one growing region, no clone should make up any more than 15% of the plantings in any given year. Empirical research on commercial plantations will probably be the only practical way to refine these recommendations. While we believe that host plant resistance is an important pest management tool, other aspects of IPM also should be examined in order to effectively utilize the various approaches available and reduce the selective pressures on the target pest (Hart et al. 1992). Incorporating effective clonal deployment strategies with host plant resistance and other IPM tactics will reduce selective pressure even further. We also must remember that SRWC plantations are delicate biological systems. Systematic monitoring for the efficacy of the resistance trait is necessary, as is the continued search for potential new pests and new pest management tactics. ACKNOWLEDGEMENTS Preparation of this manuscript was sponsored by the Bioenergy Feedstock Development Program of the U. S. Department of Energy under contract DE-AC05-00OR22725 with University of Tennessee-Battelle LLC. Partial Funding was provided by the Department of Energy-Savannah River Operations office through the Forest Service Savannah River and the Forest Service Southern Research Station under Interagency Agreement DE-IA0900SR22188. We thank the book editors for inviting us to speak and write on this subject.

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Peterson, E. B., Peterson, N. M., and McLennan, D. S. 1996, Black cottonwood and balsam poplar managers’ handbook for British Columbia. FRDA Report 250. Partnership Agreement on Forest Resource Development: FRDA II. 116 p. Picard, S., Chenault, J., and Augustin, S. 1994a. Short time induction defense of a Leuce poplar clone (P. tremula x P. tremuloides) against Chrysomela tremulae – propagation and evolution. Acta Horticulturae 381:540–543. Picard, S., Chenault, J., Augustin, S., and Venot, C. 1994b. Isolation of a new phenolic compound from leaves of Populus deltoides. Journal of Natural Products 57:808–810. Pimental, D. 1995. Amounts of pesticides reaching target pests: environmental impacts and ethics. Journal of Agricultural and Environmental Ethics 8:17–29. Pope, S. M. and Nebeker, T. E. 2002. The effect of temperature on total developmental time of the cottonwood leaf beetle (Coleoptera: Chrysomelidae) in Mississippi. Environmental Entomology. (Submitted). Pullman, G. S., Cairney, J., and Peter, G. 1998. Clonal forestry and genetic engineering: where we stand, future prospects, and potential impacts on mill operations. TAPPI Journal 81:57–64. Raffa, K. F. 1989. Genetic engineering of trees to enhance resistance to insects. Bioscience 39:524–534. Raffa, K. F., McCown, B. H., Ellis, D. D., Ramachandran, R., Robison, D., and Zeldin, E. 1991. Prospects and approaches for transgenic pest resistance in energy trees, pp. 98-106, in Proceedings of the International Energy Agency Meetings in Ames, Iowa and Vancouver, British Columbia. R. B. Hall, R. D. Hanna, and R. N. Nyong’o (eds.). Iowa State University Press, Ames, Iowa, USA. Raffa, K. F., Kleiner, K. W., Ellis, D. D., and McCown, B. H. 1997. Environmental risk assessment and deployment strategies for genetically engineered insect-resistant Populus, pp. 249–263, in Micropropagation, Genetic Engineering, and Molecular Biology of Populus. N. B. Klopfenstein, Y. W. Chun, M. -S. Kim, and M. R. Ahuja (eds.). M. C. Dillon, R. C. Carman, and L. G. Eskew (tech. eds.). Gen. Tech. Rep. RM-GTR-297. Fort Collins, CO: U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station. 326 p. Ramachandran, R. 1993. Biotechnology and host-plant resistance: Benefits, risks, and strategies for development and deployment, pp. 275-288, in Chemical Ecology of Phytophagous Insects. T. N. Anathakrishnan and A. Raman, (eds.). Science. 388 p. Roberds, J. H. and Bisher, J. W. 1997. Risk analyses in clonal forestry. Canadian Journal of Forest Research 27:425-432. Robison, D. J., McCown, B. H., and Raffa, K. F. 1994. Responses of gypsy moth (Lepidoptera: Lymantriidae) and forest tent caterpillar (Lepidoptera: Lasiocampidae) to transgenic poplar, Populus spp., containing a Bacillus thuringiensis gene. Environmental Entomology 23:1030– 1041. Root, R. B. 1973. Organization of a plant-arthropod association in simple and diverse habits: the fauna of collards (Brassica oleracea). Ecological Monographs 43:95–124. Roth, S., Lindroth, R. L., Volin, J. C., and Kruger, E. L. 1998. Enriched atmospheric and defoliation: effects on tree chemistry and insect performance. Global Change Biology 4:419–430. Royle, D. J., Hunter, T., and McNabb, H. S., Jr. 1998. Diseases and pests in biomass production systems, pp. 105–118, in Proceedings of the International Energy Agency Bioenergy Task XII Workshop, Accomplishments in Bioenergy Production Research 1995–1997. R. Gambles and G. Page (eds.). Ryan, C. A. 1981. Proteinase inhibitors, pp. 351–370, in The Biochemistry of Plants. A. Marcus (ed.). Vol. 6. New York: Academic Press. Ryan, C. A. 1990. Proteinase inhibitors in plants: genes for improving plant defenses against insects and pathogens. Annual Review of Phytopathology 28:425–449. Sage, R. B., and Tucker, K. 1997. Invertebrates in the canopy of willow and poplar short rotation coppices. Aspects of Applied Biology 49:105–111. Sage, R. B., Fell, D. A., Tucker, K., and Sotherton, N. W. 1999. Post hibernation dispersal of three leafeating beetles (Coleoptera: Chrysomelidae) colonising cultivated willows and poplars. Agricultural and Forest Entomology 1:61–70. . Schuette, B. 2000. Weed management strategies for hybrid poplar plantings, pp. 83–86, in Hybrid Poplars in the Pacific Northwest: Culture, Commerce, and Capability. K. A. Blatner, J. D. Johnson, and D. M. Baumgartner (eds.). Symposium Proceedings, 7-9 April 1999, Pasco, WA. Washington State University Cooperative Extension Publication MISC0272, Pullman, WA. 115 p.

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Shea, K. R. 1971. Disease and insect activity in relation to intensive culture of forests, pp. 109–118, in Proceedings of the XV International Union of Forest Research Organizations (1UFRO). USDA Forest Service, U.S. Department of Agriculture. Solomon, J. D. 1988. Observations on two Papaipema borers (Lepidoptera: Noctuidae) as little known pests of intensively cultured hardwood trees. Journal of Entomological Science 23:77–82. Solomon, J. D., and Abrahamson, L. P. 1972. Hardwood nursery insects, pp. 28–33, in Proceedings of the Southeastern Nurseryman’s Conference. USDA Forest Service, Southeastern Area, State and Private Forestry. Stettler, R. F., Zsuffa, L., and Wu, R. 1996. The role of hybridization in the genetic manipulation of Populus, pp. 87–112, in Biology of Populus and its Implications for Management and Conservation. Part I, Chapter 4. R. F. Stettler, H. D. Bradshaw, Jr., P. E. Heilman, and T. M. Hinckley (eds.). NRC Research Press, National Research Council of Canada, Ottawa, ON, Canada. 539 p. Stewart, J. W., and Payne, T. L. 1975. Seasonal abundance and impact of the cottonwood twig borer on cottonwood trees. Journal of Economic Entomology 68:599–602. Strauss, S. H., Rottman, W. H., Brunner, A. M., and Sheppard, L .A. 1995. Genetic engineering of reproductive sterility in forest trees. Molecular Breeding 1:5–26. Strauss, S. H., Meilan, R., Difazio, S. P., Mohammed, R., Brunner, A. M., Leonardi, S., Skinner, J. S., and Krutovskii, K. 1998. Tree Genetic Engineering Research Cooperative Annual Report: 1997-98. Forest Research Laboratory, Oregon State University, Corvallis. 45 pp. Tabashnik, B. E. 1994. Evolution of resistance to Bacillus thuringiensis. Annual Review of Entomology 39:47–79. Tabor, G. M., Kubisiak, T. L., Klopfenstein, N. B., Hall, R. B., and McNabb, H. S., Jr. 2000. Bulked segregant analysis identifies molecular markers linked to Melampsora medusae resistance in Populus deltoides. Phytopathology 90:1039-1042. Tang, J. D., Collins, H. L., Metz, T. D., Earle, E. D., Zhao, J. Z., Roush, R. T., and Shelton, A. M. 2001. Greenhouse tests on resistance management of Bt transgenic plants using refuge strategies. Journal of Economic Entomology 94:240–247. Thomas, J. B., and Rose, A. H. 1979. Insect damage to hybrid poplar plantings, 6 p., in Poplar Research, Management, and Utilization in Canada. D. C. F. Fayle, L. Zsuffa, and H. W. Anderson, (eds.). Ontario Ministry of Natural Resources, Forest Research Information Paper No. 21. van Oosten, C. 2000. Hybrid poplar management in coastal British Columbia and northwest Washington, pp. 39–42, in Hybrid Poplars in the Pacific Northwest: Culture, Commerce, and Capability. K. A. Blatner, J. D. Johnson, and D. M. Baumgartner (eds.). Symposium Proceedings, 7-9 April 1999, Pasco, WA. Washington State University Cooperative Extension Publication MISC0272, Pullman, WA. 115 p. Wang, G., Castiglione, S., Chen, Y., Li, L., Han, Y., Tian, Y., Gabriel, D. W., Han, Y., Mang, K., and Sala, F. 1996. Poplar (Populus nigra L.) plants transformed with a Bacillus thuringiensis toxin gene: insecticidal activity and genomic analysis. Transgenic Research 5:289–301. Waterman, A. M. 1946. Canker of hybrid poplar clones in the United States caused by Septoria musiva. Phytopathology 35:148–156. Wilson, L. F. 1979. Insect pests of Populus in the Lake States, pp. 75–81, in Proceedings of the North American Poplar Council. Thompsonville, MI. Woessner, R. A., and Payne, T. L. 1971. An assessment of cottonwood twig-borer attacks. Proceedings of the Southern Conference on Forest Tree Improvement 11:98–l 07. Zsuffa, L., Giordano, E., Pryor, L. D., and Stettler, R. F. 1996. Trends in poplar culture: some global and regional perspectives, pp. 515–539, in Biology of Populus and its Implications for Management and Conservation. R. F. Stettler, H. D. Bradshaw, Jr., P. E. Heilman, & T. M. Hinckley (eds.). Part II, Chapter 20. NRC Research Press, National Research Council of Canada, Ottawa, ON, Canada. 539 p. Zsuffa, L., Sennerby-Forsse, L., Weisgerber, H., and Hall, R. B. 1993. Strategies for clonal forestry with poplars, aspens, and willows, pp. 91–119, in Clonal Forestry. II. Conversation and Application. Genetics, Biotechnology, and Application. M. R. Ahuja and W. J. Libby (eds.). Springer-Verlag, Berlin, Heidelberg. 240 p.

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CHAPTER 10 STRATEGIES FOR DEPLOYMENT OF INSECT RESISTANT ORNAMENTAL PLANTS Substantial Hurdles, Vast Potential

DANIEL A. HERMS

Department of Entomology, The Ohio State University, Ohio Agricultural Research and Development Center, 1680 Madison Ave., Wooster, OH 44691 USA

1. INTRODUCTION In the 50 years since Painter (1951) published his landmark treatise, host plant resistance (HPR) has become a central component of IPM programs for many agronomic crops (e.g. Beck, 1965; Gracen, 1986; Smith, 1989; Stoner, 1996). HPR has also long been recognized as an ideal pest management strategy for ornamental plants and shade trees (Felt, 1905; Houser, 1918; Weidhaas, 1976; Morgan et al., 1978; Nielsen, 1989). Despite this great potential, Weidhaas (1976) questioned whether host plant resistance was a practical goal. His pessimistic forecast has been confirmed, as little progress has been made over the past 25 years. Deployment of resistant germplasm remains virtually ignored as a management tool for insect pests in urban forests and ornamental landscapes (Morgan et al., 1978; Nielsen, 1989; Raupp et al., 1992). Recent trends provide reasons for optimism. As social and regulatory pressures act to decrease the use of pesticides in urban areas (Shaw, 1998), host plant resistance is receiving increased attention from researchers and appreciation from the horticulture industry as a pest management tool for ornamental plants (e.g. Aker, 1998). In this chapter, I review the progress that has been made toward development and deployment of insect resistant ornamental plants, as well as toward understanding the effects of environmental stress and cultural practices on expression of resistance. 217 M.R. Wagner et al. (eds.), Mechanisms and Deployment of Resistance in Trees to Insects, 217–237. © 2002 Kluwer Academic Publishers. Printed in the Netherlands.

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2. FACTORS CONSTRAINING THE DEPLOYMENT OF INSECT RESISTANT ORNAMENTAL PLANTS A number of reasons have been cited as justification for increased emphasis on development of pest resistant ornamental plants, including the great economic value of shade trees and ornamental plants as well as the high cost of their maintenance (Potter, 1986; Wu et al., 1991; Raupp et al., 1992), the desire to decrease pesticide applications in urban areas (Olkowski et al., 1976; Raupp et al., 1992; Shaw, 1998), the potential long-term effectiveness of HPR, and its low cost of implementation once resistant plants are developed (Weidhaas, 1976; Santamour, 1977). However, a number of factors have constrained the development and deployment of host plant resistance (Weidhaas, 1976; Morgan et al., 1978; Nielsen, 1989; Raupp et al., 1992). Historically, nurseries have experienced very little demand from the market place for insect resistant plants, and plant improvement programs have focused largely on ornamental traits such as flower color and growth habit (e.g. Erstad & Hansen, 1990). Because ornamental plants are valued for their beauty and appearance, resistance must be very effective to be a viable pest management tool. Pest populations must be maintained below thresholds that mar aesthetic appearance, which may be far lower than those that decrease growth or otherwise physiologically impact the plant (Sadof & Raupp, 1997). The great diversity of ornamental plants and their associated pests (e.g. Johnson & Lyon, 1988) also complicates efforts to develop resistant plants. Many species are plagued by multiple key pests, and genotypes resistant to one may lack resistance to others (Weidhaas, 1976). This tremendous biodiversity has also diluted efforts of the few researchers focused on insect resistance of woody ornamental plants. Few systems attract the attention of more than one researcher, and resources are insufficient to investigate the vast majority of plant-insect interactions. Furthermore, there has been little logistical and funding support for the long-term, interdisciplinary research programs necessary to develop and evaluate insect resistant trees (Hanover, 1975; Morgan et al., 1978; Nielsen, 1989). 3. DEVELOPMENT AND IDENTIFICATION OF INSECT RESISTANT GERMPLASM Despite these constraints, progress is being made. For example, insect resistance has been a primary objective of the breeding and selection program of the U.S. National Arboretum (Santamour, 1977; Aker, 1998). Of the three primary approaches for developing insect resistant germplasm, evaluating existing genotypes for resistance has more potential, at least in the short-term, than does classical breeding (including hybridization) or genetic engineering. A review of the literature reveals a substantial acceleration over the last 10 years in the screening of ornamental plants for insect resistance (see Section 3.3).

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3.1 CLASSICAL BREEDING There are numerous examples in which classical breeding has been used successfully to generate insect resistant agricultural plants (e.g. Gracen, 1986; Smith, 1989; Stoner, 1996). However, due to lack of funding and logistical difficulties associated with conducting long-term, multidisciplinary research, classical breeding (including hybridization) of woody plants specifically for insect resistance has received very little attention (Hanover, 1975; Raupp et al., 1992). Breeding of woody plants for disease resistance has received more attention (e.g. Santamour, 1977; Aker, 1998), with attempts to develop Dutch elm disease resistant elms (Ulmus) at the forefront of these efforts (e.g. Karnosky, 1979; Ware, 1992). Many of these elm genotypes have now been screened for resistance to key insect pests (see Table 1, Section 3.3). 3.2 TRANSGENIC TREES The potential benefits and risks of enhancing insect resistance of trees through genetic engineering are well recognized (Raffa, 1989; Strauss et al., 1991; Rogers & Parkes, 1995). However, genetic modification of ornamental plants for insect resistance has received little attention. Most woody plants that have been genetically modified for insect resistance, such as hybrid poplars (Populus) (Robison et al., 1994) and some fruit trees (Snow & Palma, 1997), are not widely used as ornamental plants or shade trees. Sweetgum (Liquidambar styraciflua), which is commonly planted as a shade tree, is an exception. Sweetgums that were genetically modified to over-express tobacco peroxidase showed higher levels of resistance to gypsy moth (Lymantria dispar) than did wild-type trees (Dowd et al., 1998). Genetic engineering clearly offers great potential for enhancing insect resistance of ornamental plants, but current backlash against transgenic crops suggests that the public may not be ready to accept genetically modified ornamental plants. Furthermore, many ornamental plants are themselves native species, or have close relatives among the native flora, creating potential for gene flow from geneticallymodified ornamental species to their wild relatives (Rogers & Parkes, 1995; Snow & Palma, 1997). This risk is further aggravated by the long-lived nature of woody plants, coupled with the fact that many are cultivated specifically because of the ornamental value of their reproductive structures, although this problem potentially could be mitigated by insertion of genes that confer sterility. 3.3 SCREENING FOR RESISTANCE Horticulturists have selected and bred for substantial genetic diversity within many taxa of ornamental plants, much of which is maintained through asexual propagation. Screening existing genotypes represents a practical and cost-effective opportunity for identification and deployment of insect resistant germplasm (Santamour, 1977; Raupp et al., 1992). Smith-Fiola (1995) compiled a

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comprehensive list of ornamental plants for which published claims of insect and disease resistance have been made. However, not all of these claims have been substantiated by rigorous screening. An example of the pitfalls of resistance claims based on observational evidence is discussed below. Peer-reviewed studies in which woody ornamental plants were screened for their resistance to key insect pests have increased substantially in recent years, and are catalogued in Table 1. Virtually all reveal substantial variation in insect resistance. Many taxa have also been evaluated for their suitability as hosts to gypsy moth (Peterson & Smitley, 1991; Liebhold et al., 1995), which is an increasingly important pest in urban forests as it continues to expand its range in the United States (Czerwinski & Isman, 1986; Ticehurst & Finley, 1988). Although screening creates potential for immediate deployment of resistant germplasm in ornamental plantings and urban forests, there is little evidence that host plant resistance has yet to be adopted as a pest management strategy.

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3.3.1 CASE STUDY: THE SEARCH RESISTANT WHITE-BARKED BIRCHES

FOR

BRONZE

BIRCH

BORER

In a rigorous example of resistance screening, David G. Nielsen has conducted a 20year, large-scale field study of interspecific variation in birch (Betula spp.) resistance to bronze birch borer (Agrilus anxius) at The Ohio State University’s Ohio Agricultural Research and Development Center in Wooster (Nielsen & Herms, in preparation). White-barked birches are highly valued as landscape plants (Weaver, 1978; Dirr, 1981). Historically, European white birch (Betula pendula) was the most commonly cultivated birch, because it grows rapidly and develops white bark at a young age (Santamour, 1982; Schilling, 1984). However, infestations by bronze birch borer have dramatically curtailed its use in landscapes (Ball & Simmons, 1980). Larvae feed under the bark on phloem tissue, which girdles and often kills the tree (Anderson, 1944; Barter, 1957). The high susceptibility of European white birch to bronze birch borer spawned a search for

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other white birches suitable for landscapes (Dirr, 1981), with bronze birch borer resistance specified as the “single major selection criterion for landscape use” (Santamour & McArdle, 1989). Nielsen initiated his study in 1979 by planting eight species of birch (a total of 1200 trees) in a randomized complete block design. Species tested included the European species B. pendula and B. pubescens, the Asian species B. maximowicziana and B. platyphylla var. szechuanica, and the North American species B. papyrifera, B. populifolia ‘Whitespire’, and B. nigra. B. populifolia ‘Whitespire’ was initially misidentified as B. platyphylla var. japonica, which is native to Asia. Recently, chemotaxonomic and morphological evidence has confirmed its identity as B. populifolia (Santamour & Lundgren, 1996). Bronze birch borer colonization and tree mortality were quantified throughout the 1980s and again in 1999. Bronze birch borer infestations, which were first detected in the plots in 1982, had resulted in 100% mortality of B. p. var. szechuanica, B. pendula, and B. pubescens by 1986 (Table 2). Intensive quantification of larval colonization and successful adult emergence confirmed that mortality was caused by bronze birch borer. By 1990, bronze birch borer had killed 86% of B. maximowicziana, and all individuals were dead by 1999. B. papyrifera and B. populifolia ‘Whitespire’ experienced much lower levels of infestation (Table 2). Mortality of both species increased slightly between 1988 and 1990, possibly as a result of the severe 1988 drought, which triggered substantial mortality of native B. papyrifera throughout forests of the Great Lakes region (Jones et al., 1993). The minimal amount of mortality that did occur in both species between 1990 and 1999 was probably due to canopy closure in the experimental plot. Birches are early successional species intolerant of shade (Perala & Alm, 1990), and mortality was concentrated among suppressed individuals. The high rate of survival of B. papyrifera and B. populifolia ‘Whitespire’ over the 20-year study, in the face of outbreaks that killed hundreds of neighboring trees, as well as substantial droughts in 1988 and 1991 (trees were not irrigated), suggests that these native white-barked birches can be grown successfully in landscapes of the Midwestern United States. B. nigra (which does not have white bark) showed no evidence of bronze birch colonization, and virtually no mortality (Table 2), confirming its suspected immunity to bronze birch borer (Santamour, 1999).

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Theory of biogeography predicts that geographic variation in herbivore resistance corresponds with geographic patterns of natural selection exerted by key herbivores (e.g. Bryant et al., 1994; Swihart et al., 1994). The high level of resistance in the North American species coupled with complete mortality of the Asian and European species is consistent with this prediction. Bronze birch borer is native to North America, as are the species showing the highest level of resistance: B. nigra, B. papyrifera and B. populifolia. The Asian and European species, which share no evolutionary history with bronze birch borer, exhibited a very high degree of susceptibility, suffering 100% mortality. The lack of resistance in Asian and European species indicate that bronze birch borer will have a devastating impact on the birch resource on these continents, should it become inadvertently established. These results stand in stark contrast to claims of bronze birch borer resistance in B. maximowicziana and B. platyphylla as they were released to the nursery industry during the 1970s (Kozel & Smith, 1976; Santamour & Clausen, 1979; Dirr, 1981). That they were eventually proven highly susceptible underscores the pitfalls of resistance claims based on anecdotal observation and other forms of circumstantial evidence, which may represent escape from infestation rather than true resistance. Claims of resistance should be backed by rigorous screening in replicated plantings that ideally contain genotypes known to be susceptible, which can be used as “positive controls” to provide a frame of reference. Santamour and Lundgren (1997) and Santamour (1999) hypothesized that the absence of the secondary metabolite rhododendrin in the inner bark of birch was mechanistically associated with resistance to bronze birch borer, and thus could be used as a screening trait in the selection and breeding of resistant trees. This hypothesis was based on the observation that river birch (B. nigra) and monarch birch (B. maximowicziana), both of which they assumed to be borer resistant, do not contain rhododendrin, while species known to be susceptible do. However, the high level of susceptibility of monarch birch to bronze birch borer (Table 2) indicates that the absence of rhododendrin is not a reliable marker for bronze birch borer resistance, again emphasizing the importance of a rigorous long-term screening program. 4. ENVIRONMENTAL MODIFICATION OF RESISTANCE: DOES URBAN STRESS TRIGGER PEST OUTBREAKS? Plant resistance to insects results from a suite of physical and chemical traits that decrease the growth and survival of insects, the attractiveness of plants to insects, and/or the ability of plants to tolerate insect feeding (Painter, 1951). Although resistance traits are genetically based, their expression can be altered dramatically by environmental factors, including biotic and abiotic stress and cultural practices such as fertilization (Painter, 1958). A large body of predominantly observational evidence has led to the proposition that a mechanistic relationship exists between plant stress and the population dynamics of herbivorous insects that is mediated by stress effects on host quality

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(Mattson & Haack, 1987). Stress has been proposed to increase the nutritional quality and/or weaken the natural defenses of plants, thereby increasing insect fecundity and survival (Rhoades, 1983; White, 1984). This “Stress Hypothesis” is widely accepted within the horticultural industry, and management recommendations for enhancing insect resistance of trees have long emphasized cultural practices that increase tree vigor (Houser, 1918; Nielsen, 1989). However, recent reviews of empirical studies have concluded that effects of environmental stress on host plant quality are highly variable, and challenge the generality that stressed trees are more susceptible to insects (Larsson, 1989; Waring & Cobb, 1992; Koricheva et al., 1998). Relative to natural forests, urban environments are clearly more stressful (Berang et al., 1985; Krizek & Dubik, 1987; Whitlow & Bassuk, 1988; Whitlow et al., 1992; Kjelgren & Clark, 1993; Craul, 1994; Close et al., 1996a,b; Cregg & Dix, 2001). Trees in urban sites experience greater drought stress because of higher temperatures, restricted rooting zones, compacted soil, and decreased water infiltration due to impervious surfaces. Urban environments are also often characterized by soils deficient in organic matter and nutrients, air pollution, deicing chemicals, and increased incidence of mechanical injury. In natural forests, stress quickly eliminates seedlings or saplings that are not at least reasonably well adapted to the site on which they happen to establish. Trees that do become established acclimate to stress via a suite of phenotypic responses that enhance stress tolerance, including increased root:shoot ratios, increased accumulation of storage reserves, and higher concentrations of secondary metabolites (Chapin, 1991; Chapin et al., 1993). But in urban forests and ornamental landscapes, trees and shrubs are often planted with little consideration as to whether they are actually adapted to the stresses associated with the particular site (Nielsen, 1989; Raupp et al., 1992), which may dramatically decrease their ability to acclimate to stress. Numerous cases have been documented of insect outbreaks in urban forests by species that rarely, if ever, reach high densities in natural forests (Frankie & Ehler, 1978; Dreistadt et al., 1990). Stress effects on host quality have been implicated as a key causal factor (Nielsen, 1989; Dreistadt et al., 1990; McIntyre, 2000). However, the generality of this pattern has been questioned by Nuckols and Connor (1995), who found that trees in ornamental plantings did not receive more herbivory than conspecifics in natural forests (although, they did not actually quantify insect performance or other measures of host plant resistance). Only a few studies have actually examined the relationship between urban stress and insect infestation. In urban environments, Speight et al. (1998) reported that the density of horse chestnut scale (Pulvinaria regalis) was highest where water and nutrient infiltration was inhibited by impermeable surface substrate under the trees. They concluded that higher insect densities resulted because stress enhanced host quality. However, they did not examine host plant effects on fecundity or survival. In general, drought stress has been found to decrease host quality of woody plants for sucking insects (Koricheva et al., 1998). For example, Hanks and Denno (1993) found that survival of the armored scale Pseudaulacaspis pentagona on mulberry

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(Morus alba) was lower on water stressed trees in urban environments than on trees in forested sites that experienced less stress, challenging the idea that stressed trees are better hosts. Effects of drought stress on folivores also have been variable. Water stress decreased folivore performance in some cases (e.g. Craig et al., 1991; Mopper & Whitham, 1992; Floater, 1997). However, other studies reached the opposite conclusion (Thomas & Hodkinson, 1991; Cobb et al., 1997), or found effects to be minimal (McCullough & Wagner, 1987; Talhouk et al., 1990). Studies with bark beetles have also reached conflicting conclusions. In some studies, stressed trees were the most susceptible and fastest growing trees the most resistant (e.g. Larsson et al., 1983; Wright et al., 1984; Waring & Pitman, 1985). However, Lorio and his colleagues have concluded that moderately stressed loblolly pine (Pinus taeda) trees are more resistant to southern pine beetle (Dendroctonus frontalis) than are faster growing trees (Lorio, 1986; Reeve et al., 1995; Wilkens et al., 1997). Similarly, white pine weevil (Pissodes strobi) preferred to feed on bark from nonstressed white pine trees (P. strobus) over bark from drought stressed trees (Lavallée et al., 1994). It has been proposed that stress effects on insect resistance may be nonlinear, with moderately stressed trees more resistant to herbivores than either severely stressed or rapidly growing trees (Lorio, 1986; Mattson & Haack, 1987; Larsson, 1989; Herms & Mattson, 1992). The existence of quadratic effects of stress on herbivore resistance provides a potential explanation for otherwise contradictory results of stress studies (e.g. English-Loeb, 1989). While evidence for quadratic responses is very limited, there is some. For example, Lorio and his colleagues found that when moderate drought stress decreased growth of loblolly pine without affecting photosynthesis, production of constitutive levels of trunk resin increased (Reeve et al., 1995), which decreased the reproductive success of southern pine beetle. But when severe drought stress decreased both growth and photosynthesis, resin production decreased (Dunn & Lorio, 1993). Ozone may be an important predisposing stress in tree decline, particularly in urban forests (Kozlowski, 1980; Pye, 1988; Taylor et al., 1994; MacKenzie et al., 1995; Schmieden & Wild, 1995). It has been proposed that ozone stress may decrease tree resistance to insects (Hain, 1987), but this has been investigated in only a few cases. Experimental ozone fumigation decreased resistance of quaking aspen (Populus tremuloides) to four species of outbreak Lepidoptera (Herms et al., 1996), but this does not seem to be a general pattern. Ozone exposure had no effect on host quality of sugar maple (Acer saccharum) or hybrid poplar as hosts for gypsy moth (Lindroth et al., 1993). Similarly, exposure of cottonwood (Populus deltoides) to ozone had no effect on the aphid Chaitophorus populicola (Coleman & Jones, 1988a). Ozone did decrease the growth and fecundity of the cottonwood leaf beetle (Plagiodera versicolora). However, this insect preferred to feed on, and consumed more foliage of, plants exposed to elevated ozone (Coleman & Jones, 1988b; Jones & Coleman, 1988). Gypsy moth preferentially fed on white oak (Quercus alba) foliage exposed to the highest concentration of ozone (about 3X ambient), but preferred foliage exposed to ambient air over that exposed to intermediate levels of ozone (Jeffords & Endress, 1984).

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Atmospheric nitrogen deposition also imposes a substantial anthropomorphic impact on natural and urban forests (Taylor et al., 1994). Deposition of nitrogen originating from fossil fuel combustion increases available nitrogen in the soil, resulting in increased foliar nitrogen concentration of trees (Johnson, 1992; Fenn et al., 1998). Numerous studies have shown that increased nitrogen availability frequently decreases tree resistance to insects by increasing nutrient and/or decreasing secondary metabolite concentrations (Mattson, 1980; Herms & Mattson, 1992; Kytö et al., 1996). For example, in Australia, atmospheric nitrogen deposition has been implicated in the increased susceptibility of Eucalyptus forests to defoliation (Landsberg, 1990). Wood borers deserve special attention because of their often lethal impact on trees. There is substantial evidence that stressed trees are more susceptible to wood borers (e.g. Anderson, 1944; Wargo, 1977; Dunn et al., 1986; Potter et al., 1988; Dunn et al., 1990; Hanks et al., 1999). For example, Cregg and Dix (2001) found that green ash (Fraxinus pennsylvanica) planted in a downtown urban environment experienced more severe drought stress and suffered higher levels of borer damage than trees planted on a park-like campus. Consideration by landscape architects and designers of the ecological requirements and adaptations of trees when deciding where to locate plants could help reduce urban stress (e.g. Flint, 1985) and thus incidence of borer infestation. For example, flowering dogwood (Cornus florida) is an understory tree that poorly tolerates mid-day water stress compared to species adapted to full sun (Bahari et al., 1985). Not surprisingly, Potter and Timmons (1981) found that dogwood trees planted in full sun were much more susceptible to colonization by dogwood borer (Synanthedon scitula) than were trees planted in at least partial shade. It is obvious that the effects of environmental stress on tree resistance to herbivores are highly variable and complex (Larsson, 1989; Waring & Cobb, 1992; Koricheva et al., 1998). Evidence suggests that effects of stress on herbivore performance will be dependent on the outcome of the three-way interaction between (1) the type, timing, and intensity of stress (e.g. McMillin & Wagner, 1995), (2) the physiological response of the plant, and (3) the behavior, physiology, and life history of the herbivore (Mattson & Haack, 1987; Larsson, 1989; Jones & Coleman, 1991; Koricheva et al., 1998). Further research clearly is necessary before a solid predictive framework will emerge. However, it is also clear that, with the exception of wood borers, there is little evidence to support the hypothesis that urban stress generally decreases tree resistance to insects, or that stress effects on host quality are responsible for destabilizing herbivore population dynamics in urban environments. Other factors may have more important effects on the population dynamics of insect herbivores in urban forests. For example, the regulating effects of natural enemies generally may be weaker in urban forests (e.g. Houser, 1918; Frankie & Ehler, 1978; Hanks & Denno, 1993; Ruszczyk, 1996).

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5. FERTILIZATION AND TREE RESISTANCE TO INSECTS: REASSESSING AN ENTRENCHED PARADIGM Fertilization is one of the most common tree maintenance practices in ornamental landscapes (Braman et al., 1998), based in large part on the rationale that it enhances pest resistance by increasing tree vigor (Potter, 1986; Rathjens & Funk, 1986; Neely & Himelick, 1987; Nielsen, 1989; Iles, 2000). However, there is little evidence to support this claim (Raupp et al., 1992). Indeed, in a recent review, Kytö et al. (1996) concluded that “where a statistically significant effect of (nitrogen) fertilization on insect performance (body size, development time, survival) was recorded, it was nearly always beneficial for the insects.” Fertilization has been shown, for example, to decrease tree resistance to spider mites (Wermelinger et al., 1985), aphids (Wainhouse et al., 1998), scales (McClure, 1980), adelgids (McClure, 1991), caterpillars (Bryant et al., 1987; Mason et al., 1992), sawflies (Popp et al., 1986; Wainhouse et al., 1998), leaf beetles (Lawler et al., 1997), leafminers (Marino et al., 1993), and browsing mammals (Nams et al., 1996), as well as shoot and stem borers, including Nantucket pine tip moth (Rhyacionia frustrana) (Ross & Berisford, 1990) and white pine weevil (Xydias & Leaf, 1964). Recent evidence also indicates that fertilization may also decrease loblolly pine resistance to bark beetles by decreasing constitutive resin flow (Wilkens et al., 1997; Warren et al., 1999), which has been shown to affect the reproductive success of southern pine beetle (Reeve et al., 1995). In general, the beneficial effects of fertilization on herbivores have been associated with fertilization-induced increases in plant nitrogen content and decreases in secondary metabolite concentrations (Mattson, 1980; Bryant et al., 1983; Herms & Mattson, 1992; Kytö et al., 1996). However, not all studies found fertilization to decrease the resistance of woody plants to insects, or to decrease secondary metabolite concentrations. For example, in extremely nutrient deficient forests, fertilization of jack pine (P. banksiana) (McCullough & Kulman, 1991) and Scots pine (Pinus sylvestris) (Björkman et al., 1991) increased foliar nitrogen and monoterpene concentrations. Sawfly performance was not affected in either study, perhaps because negative effects of increased terpene concentrations on host quality were offset by positive effects of increased foliar nitrogen. In summary, there is little evidence to support the paradigm entrenched within the tree care industry that fertilization enhances insect resistance of trees. In fact, substantial evidence demonstrates that fertilization almost always decreases tree resistance to herbivores. 6. SUMMARY Host plant resistance has been recognized as an ideal pest management strategy for ornamental plants and shade trees for many years. Yet, little progress has been made in the deployment of resistant germplasm in urban forests and ornamental landscapes. A number of factors have constrained the development and deployment of insect resistant ornamental plants, including lack of market demand for insect resistant plants, and low pest thresholds for plants valued for their aesthetic

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appearance. The great diversity of ornamental plants and their associated pests both complicates efforts to develop resistant plants and dilutes the efforts of the few researchers working in this area. Furthermore, there has been little logistical and funding support for the long-term, interdisciplinary research programs necessary to breed and evaluate insect resistant ornamental plants. The future looks brighter. Horticulturists have selected and maintained substantial genetic diversity, which provides a golden opportunity for identification, selection, and deployment of insect resistant species and cultivars. Indeed, this genetic variation increasingly is being screened for insect resistance. Claims of resistance should be rigorously substantiated, as erroneous claims based on observational evidence have plagued the landscape industry in the past. Although resistance traits are genetically based, their expression can be altered dramatically by the environment. It has been widely accepted within the landscape industry that stressed plants are more susceptible to insects, and IPM programs have emphasized cultural practices that increase tree vigor. Furthermore, effects of urban stress on tree resistance to insects is frequently cited as triggering outbreaks of insects in urban forests that rarely, if ever, reach high densities in natural forests. However, experimental evidence does not support this generality. The effects of environmental stress on tree resistance to herbivores are highly variable and complex. With the exception of wood borers, there is little evidence that urban stress generally decreases tree resistance to insects, or that stress effects on host quality are responsible for destabilizing herbivore population dynamics in urban environments. In many cases, stressed trees were found to be more resistant to insects. Nor is there evidence to support the entrenched paradigm that fertilization enhances pest resistance by increasing tree vigor. Indeed, the vast majority of studies conclude that fertilization favors insects and mites, although some have found that fertilization had no effect on tree resistance to insects. I am not aware of any studies that show fertilization to increase the resistance of trees to herbivores. In 1976, Weidhaas questioned whether host plant resistance was a practical goal for shade trees and other ornamental plants. So far, his pessimistic forecast has been confirmed. Little progress has been made in the deployment of resistant germplasm. However, research focused on identification of insect resistant germplasm, as well as understanding how environmental stress and management practices impact the expression of resistance, has accelerated. There is also evidence that the value of host plant resistance as a pest management tool is increasingly appreciated by the Green Industry. These trends provide reason for optimism that the next 25 years will see substantial progress towards unleashing the vast potential of host plant resistance as a management tool for insect pests in urban forests and ornamental landscapes.

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CHAPTER 11 POSSIBILITIES TO UTILIZE TREE RESISTANCE TO INSECTS IN FOREST PEST MANAGEMENT IN CENTRAL AND WESTERN EUROPE

C.M.HEIDGER

(1)

AND F.LIEUTIER

(2)

(1) Hochschule Zittau/Goerlitz (FH) Univ.of Applied Sciences,Dept.of Ecology and Environmental Management, P.O.Box 261, D-02755 Zittau, Germany. (2) Univ. Orléans , Laboratoire de Biologie des Ligneux et des Grandes Cultures, B.P. 6759, F. -45067 Orléans Cedex, France.

1.

INTRODUCTION

Temperate forest ecosystems are the historic natural vegetation in Central and Western Europe. Broad leaved trees are dominant (Ellenberg, 1996). Beech (Fagus sylvatica) is dominant in all stands with average moisture and soil condition. Under dryer conditions, such as in the lowlands, oak species (Quercus robur and Quercus petraea) are dominant. Only under very unfavorable dry or wet conditions pine (Pinus sylvestris) occurs as natural stands. Spruce (Picea abies) only occurs in the higher altitudes, as in the Alps or the Bavarian forest and reaches its maximum western natural distribution in the lowlands at the river Wisla (Ellenberg, 1996). Presently in Central Europe the actual forests in large areas do not consist of historic natural vegetation, but of plantations in which broad leaved trees in the last centuries have been replaced by spruce and pine over a large range. Therefore the former dominance of broad leaved trees was converted to one of conifers (Plachter, 1991). In Western Europe, Great Britain and Ireland most forest stands were converted to arable land and the rest of the forests mainly consist of plantations. In France also, broad leaved trees were replaced by spruce and pine through forestry, but also in many locations broad leaved trees were planted in their natural distribution range. So even if planted, the French forests correspond in many places 239

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to the natural vegetation. Conifers have been planted especially in mountain areas, but sometimes, as in the Massif Central, in the place of broad leaved trees in low mountain areas. Also, as in central Europe, even at very low altitudes, conifers have replaced broad leaved trees in large areas such as in the southeast in place of Quercus ilex and Quercus suber and in the region of Orleans in place of Q. petraea and Q. robur. Consequently, the most relevant forest trees for our discussion of resistance in Central and Western Europe presently are Norway spruce (Picea abies), Scots pine (Pinus sylvestris), Maritime pine (Pinus pinaster), beech (Fagus sylvatica) and several oak species (Quercus petraea, Q. robur, Q. pubescens, Q. suber, Q. ilex). In this area, those species are attacked by several pests among which the most aggressive belong to the bark beetles, weevils and Lepidoptera, and to a lesser extent, aphids and scale insects (Table 1). Damage can be considerable. For example, in the beginning of the 90´s, the bark beetle Ips typographus killed over 30 million of spruce in 2-3 years, which can be estimated at a loss of about 750 million Euros. In the 70`s, the Mediterranean scale Matsucoccus feytaudi Duc. has been responsible for the destruction of most maritime pine plantations in Southeastern France. The pine processionnary moth Thaumetopoea pityocampa causes periodic damage in Mediterranean pines. Generally, broadleaved trees are less damaged than conifers, although defoliators such as Tortrix viridana or Lymantria dispar can cause spectacular outbreaks on oak. Trees however, as all living organisms, are able to defend themselves against biotic aggressions, at least to some extent. They have developed resistance mechanisms against all of these insects and the existence of more or less long periods without damage proves that these natural mechanisms are efficient most of the time. It could thus be an efficient and environmentally friendly strategy for the forester, in the context of pest management in a sustainable forest, to try and utilize these resistance mechanisms to control insect pests and to improve forest health. In the present chapter, after briefly reviewed the main mechanisms of resistance in trees and the factors which can make resistance levels vary, we suggest possibilities to utilize tree resistance for forest protection and give examples of such utilization for Central and Western European forest pests. 2.

MAIN MECHANISMS OF RESISTANCE IN TREES

These mechanisms depend essentially on the location of damage in the host and the feeding behavior of the pest (defoliator, sap-sucking, phloem feeders, xylophagous). In Central and Western Europe, several investigations in this field have been undertaken for the insects in Table 1, revealing different kinds of plant resistance mechanisms, which range from avoiding the pest to constitutive and induced local or systemic defense.

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2.1 AVOIDING THE PEST The life cycle of the pest and that of the host must often be strictly synchronized to allow the feeding stages of the insect to find the appropriate organ of the tree at the right stage of development. If the plant develops genotypes with a different

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phenology, the coincidence between its life cycle and that of the insect is largely broken, and the sensitive pest stage cannot develop on a wide scale. A resistance is thus created in the tree by avoiding the pest attack in time. One good example is the phenological resistance of oak spp. to the green oak leafroller Tortrix viridana. In spring, the newly hatched larvae rapidly enter the flushing buds of their host to feed and develop. This is possible however, only if hatching occurs not too early for the buds to be tender enough, and not too late for the larvae not to be rejected outward by the rapidly developing foliage. The extent of damage to the foliage thus varies depending on climatic conditions which can allow phenological asynchrony between egg hatching and bud flushing from one year to another, but it also depends on the genetic characteristics of the trees. Generally, late flushing trees escape defoliation (Du Merle, 1988). However, T. viridana is able to adapt to the phenologically different oak species and ecotypes (Du Merle, 1983). This is due to genetically fixed differences in egg hatching dates, through which each green oak leafroller population is specialized on a certain phenological type of oak (Altenkirch, 1966; Rubtsova, 1977, 1981; Du Merle, 1983). Also in the case of Lymantria monacha, phenological variations of its host (Norway spruce) cause resistance, whereas late flushing individual trees are less affected by the moth. But genetic selection of the late ecotype raised the attack level of Lygaeonematus abietinus (Tenthredinidae) and caused heavy infestations by this insect (Bouvarel & Lemoine 1957). Phenological asynchrony reducing insect attack was also reported by Thielges & Campbell (1972) for Adelges abietis attacking Picea abies. The strategy of avoiding the pest could be used for applied purposes in Europe by creating, enhancing or preserving the phenological variability among tree species in heterogeneous stands under the precondition that the different phenological types are genetically fixed and therefore can be used in genetic improvement programs. For example, the bud flushing date with respect to control of T. viridana populations can vary in such a way among the trees that the average phenological coincidence between the pest and its host will constantly be as low as possible (Du Merle, 1988). However it was found by Schütte (1957) that this strategy was not offering much safety against an outbreak of T. viridana.

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2.2 CONSTITUTIVE ( PREFORMED) RESISTANCE The structures and processes involved in constitutive resistance exist before attacks occur. Various physical or chemical structures can be involved, but chemically mediated resistance plays the most important role. In conifers, mainly terpenes and phenols are involved. These chemicals counteract insect attacks and are involved in defence against a wide array of aggressors, be they xylophagous, sap-suckers or defoliators. The genera Pinus, Picea, and Larix possess a system of resin ducts in phloem and xylem which contain the primary resin (Bannan, 1936). It consists of axial ducts in the wood and radial ducts in the phloem and xylem. Such primary resin ducts can function for 25 years and are responsible for the primary defence reaction against bark beetle attack (Reid et al., 1967; Berryman, 1972). In addition to resin terpenes, phenols located in phloem parenchyma cells can also play an important role in constitutive resistance against bark beetles, and between clone differences have been demonstrated for stilbenes and flavonoids (Brignolas et al., 1995; Franceschi et al., 1998) (See also Lieutier, this volume). Constitutive resistance of Pinus pinaster against the pyralid stem borer Dioryctria sylvestrella is also genetically determined and terpinolene could be used to select resistant genotypes of the host species (Jactel et al., 1999), since the attacks are always most severe on trees with high levels of terpinolene in their volatile emissions. In P. pinaster, investigations on the survival after natural infestation by the scale Matsucoccus feytaudi have also demonstrated a high between-provenance variability in host resistance (Schvester & Ughetto, 1986). Another example for a sap sucker is given by the green spruce aphid Elatobium abietinum; its performances varied with provenance of Picea sitchensis (Day et al., 1999). In most cases, the best growing provenances were the most resistant ones and insect performance was related to variations in stilbenes. A relation even existed between aphid infestation and the bark consumption rate by the bole weevil Hylobius abietis; the more aphids found on the provenance, the higher was the amount of bark consumed by the weevil (Day et al., 1999). In Pinus sylvestris, several families of phenolic compounds have been characterized (Popoff & Theander, 1977; Niemann, 1979). The toxic effects of the phenolic content of the foliage from different clones on insects were described by Thielges (1968) and several other authors and these compounds have been reported often to be involved in defence mechanisms against defoliating insects (Lunderstädt, 1976, Harborne, 1985). Females of the European pine sawfly Diprion pini oviposit on different clones of P. sylvestris, but significant host preferences among clones have been demonstrated. Rohmeder (1954) and Wright & Wilson (1967) found differences among Scots pine varieties in susceptibility to this insect. Egg and larval survival varied significantly between clones (Pasquier-Barré & Auger-Rozenberg, 1999). As taxifolin is known as an anti-growth-chemical for insects (Elliger et al., 1980), absence and presence of taxifolin in different clones were studied (Lebreton et al. 1990; Yazdani & Lebreton, 1991). Auger et al. (1994) found that high rates of mortality of D. pini occurred when Scots pine needles contained high concentrations

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of taxifolin and taxifolin glucosid. Also, it could be shown that resistant clones that were toxic for D. pini contained taxifolin (Géri et al., 1994). Those clones were also toxic for the processionnary caterpillar Thaumetopoea pityocampa and the larvae of the endangered butterfly Graellsia isabellae. Preformed resistance also occurs in broad leaved trees. For example, Schopf et al. (1999) found that the performance of Lymantria dispar was better on Quercus cerris than on Q. petraea. Constitutive resistance could be used in genetic improvement programs by selecting clones with high levels of defence chemicals. However, it is not clear yet if plants with raised levels of defence chemicals are of practical use because there is still a lack of information on the genetic differences between the populations of pest insects and on the reaction of natural enemies of the pest species. 2.3 LOCAL INDUCED DEFENCE In the case of local induced defence, the structures involved in these resistance mechanisms are expressed only in response to attack, and this response is located in the tissues situated in close vicinity to the place of attack. As for constitutive defenses, all kind of structures can be involved but the chemically mediated mechanisms generally play the most important role. Local induced defence is also known to act against various kinds of insect guilds. Trees react to attack by microorganisms such as bark beetle vectored fungi with the formation of a necrotic zone around the attack area, both in the phloem and the sapwood. This is considered as a hypersensitive reaction (Berryman, 1972; Christiansen et al., 1987). The resistance of conifers to bark beetle attack depends mainly on the efficiency of these induced local reactions. The reaction seems to be induced by wounding itself, but also the fungi introduced by the beetle into the wound can stimulate considerably the development of the reaction (Lieutier et al., 1995). Drastic changes in phytochemical contents occur in the lesion zone formed in the tissues around the attack site, especially in phenolics and terpenes. These chemicals stop the attack by the insect and its associated fungus (Reid et al., 1967; Berryman, 1969; Raffa and Berryman, 1982; Langström et al., 1992; Lieutier et al., 1996). According to Christiansen et al. (1999), a Norway spruce tree attacked by Ips typographus vectored fungus Ceratocystis polonica forms a circle of axial traumatic resin ducts in the xylem of the stem which produces secondary so called wound resin. The resistance level of P. abies to Ceratocystis polonica is correlated with the concentration of resin in the phloem necroses (Christiansen et al., 1987). Trees with a high production of in the reaction zone are less susceptible to bark beetle attack (Birgerson, 1989). The resistance is also correlated with a particular phenolic composition in the reacting tissues, especially with the ability of the tree to rapidly increase catechin synthesis in the phloem reaction zone (Brignolas et al., 1995, 1998). Christiansen et al. (1999) also discovered that a Norway spruce tree that survived bark beetle attack could be more resistant because traumatic resin ducts formed in the delayed induced reaction described above already existed (For induced defences against bark beetles see also Lieutier, this volume).

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Like in bark beetles, local induced defence could be of greater importance than constitutive defence in the resistance of P. abies to Pissodes strobi (Lavallée et al., 1999). Although better known and much more frequent against attacks by xylophagous insects, local induced defense has also been demonstrated to play a decisive role in trees attacked by other insect guilds. The resistance of a certain Norway spruce tree to the females and larvae of the aphid Adelges abietis is related to the capacity of the tree to rapidly develop a local induced reaction in the buds around the zone where the fundatryx nymph has inserted its mouth parts (Rohfritsch, 1988). Local induced defence of trees could be used by selecting or genetically engineering plants with strong and fast responses to aggressor attacks. Also the formation of traumatic resin ducts could be used if it would be possible to induce it in a way that the tree survives with an increased resistance. This could function as a “vaccination” for endangered stands. 2.4 SYSTEMIC INDUCED DEFENCE Systemic induced defence results in stimulation of the defence mechanism only after attack begins. The situation however completely differs from the local induced defence because the structures or processes concerned are dispersed in the whole tree instead of being localized at the point of aggression, as insect attacks can modify the metabolics of phenolics in the whole plant (Wagner, 1988). Due to this the content of the defence chemicals is raised in the whole plant after attack. A good example is the resistance of Larix decidua to the larch bud moth Zeiraphera diniana in the Alps. Periodic outbreaks of this moth could be explained by induced defence responses of the trees after heavy defoliation. The new needles growing after heavy defoliation contain more non-digestible fiber material and less nitrogen than the needles prior to heavy defoliation. This results in reduced food quality for later moth generations and could play a considerable role in the collapse of the outbreak (Roques, 1983). It can therefore be called a delayed induced systemic reaction. Combined effects of preformed (constitutive) defence and systemic induced defence were found in the resistance of different clones of Pinus sylvestris to Diprion pini by Auger et. al (1994). During feeding tests or defoliation a strong increase in taxifolin glucoside occurred in the needles which was correlated with tree resistance. Induced systemic responses could be used in genetic improvement programs by selecting clones with strong and fast responses in conventional breeding programs, or by raising levels of such defences in the plants using genetic engineering. 3. FACTORS INFLUENCING TREE RESISTANCE AND CONSEQUENCES FOR UTILIZATION IN FOREST PEST MANAGEMENT Very few practical attempts have been made to use tree resistance mechanisms in forest pest management, but there are several examples in research to clarify

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whether those mechanisms can be a tool in forestry. This is a rather difficult task because the phenotypic response of the tree species to a pest species is determined by the interaction of different major factors, which also influence the resistance level of a tree. Four categories of factors must be considered: 1) the genetic information in the tree; 2) the genetic information in the pest species; 3) the genetic information in the pathogens introduced by the pest species; 4) the environmental conditions (moisture, temperature, nutrient availability, air pollution, soil conditions, competition). In most investigations, the genetic information in the tree has been investigated by tests with clones or provenances and, as seen above, many examples of tree resistance to insects have been demonstrated. However, as emphasized by Bastien (1999), only a few investigations so far have taken into account the genetic variability of the insect pests themselves and the pathogens introduced by the pest species. An example of this is the genetically differing populations of the defoliator T. viridana specialized on different phenological oak types as pointed out above. Several investigations in that field are presently being conducted in Europe on other pest guilds, such as cone and seed insects, sap suckers and bark beetles. Environmental conditions also influence the level of tree resistance, making silvicultural practices a potentially important tool to enhance resistance of forest trees. For example, a susceptible host can become more resistant due to favorable environmental conditions (e.g. weather) (Lévieux, 1986). This resistance, called pseudo-resistance, lasts only as long as optimal conditions continue, and is therefore temporary. In Southern and Central England almost all individuals of Pinus contorta are attacked by Rhyacionia, but in Scotland the same provenances are not attacked, thus reflecting the role of environmentally induced pseudo-resistance (Lévieux, 1986). In this case, the effects of climate impact the performance of the pest, leading to a situation of resistance in a susceptible provenance. Also, adverse effects from climate can occur, as in the case of bark beetle attacks in Central Europe, where warmer climatic conditions allow the bark beetle Ips typographus to produce more offspring (2 generations per year) than in the natural distribution range of norway spruce (Heidger, 1994). More trees, even resistant ones, can be attacked due to higher population levels (Vité, 1984). Another example concerns Tomicus piniperda. In Northern Europe extensive tree mortality is very rare because attacks are localized in the shoots only (Langström et al., 1992), but in the warmer climate of Southern Europe stem attacks and tree mortality occur (Triggiani, 1984). Consequently, two main possibilities can be considered for the utilization of tree resistance in forest pest management: 1) tree breeding for genetic resistance, by taking into account resistance criteria in genetic improvement programs; and 2) enhancement of the resistance level and efficiency of defense mechanisms in the trees with the aid of silvicultural practices that optimize environmental conditions.

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4. ENHANCEMENT OF RESISTANCE BY GENETIC IMPROVEMENT PROGRAMS Some of the resistance mechanisms described above offer the possibility to select resistant clones for genetic improvement of resistance to insects. However, breeding for resistance to biotic aggressors is much more complex than to abiotic factors, as sequential evolution of the pest species or plant-aggressor coevolution can take place (Holubcik, 1978). Trying to enhance resistance of trees using a single gene is problematic as resistance can easily be overcome in less than a single tree generation (Lévieux, 1986). It would thus probably be better to select horizontal resistance which is more effective over longer time periods. It has been also pointed out that often monogenic resistance mechanisms can be found, but many tree insect interactions are complex phenomena being controlled by several loci (Bastien, 1999). There are also practical restrictions for the use of clones because it could lead to restriction of genetic diversity in the tree population. A special problem is also to define against which of the different pest species of a certain tree species resistance should be raised (Führer, 1975). This is even more complicated because of the various demands of the different insects according to their feeding strategy and their age class specificity. Tree breeding programs, no matter whether they are based on classical breeding programs or on the production of transgenic plants, must thus recognize the need to achieve a durable genetic resistance against the many aggressors. Again, this is possible only if conservation of genetic variability is part of the breeding program, otherwise insects and pathogens vectored by them can easily overcome tree resistance due to their short generation cycles in comparison to those of the trees. Consequently, for all these reasons and like in agriculture, so called multiline or polyclonal cultures should only be planted as already recommended by Holubcik (1978). Another question is, which genotypes should be selected. According to Führer (1975), the selection should not be focused necessarily on the most unsuitable genotypes for the pest. Genotypes that offer it a constant food quality, even under changing environmental conditions, should be preferred. Indeed, under these conditions the pest population level would be stabilized because of both a constant food quality and a high level of natural antagonists due to the constant presence of the pest, thus avoiding mass outbreak. Such genotypes, stable or unstable under a changing environment, have already been reported to exist, for example in the xeromorphism of spruce needles regarding water availability (Führer, 1975). When selecting resistant genotypes, one must pay attention to the mechanisms involved in the resistance, especially regarding their specificity for the target species. A first clue of the problem could be the investigation by Géri et al. (1994) on Scots pine resistance to the sawfly D. pini. In performance tests on clones that were unfavorable to D. pini because of their content in certain flavonoid compounds, the larval development of the butterfly Graellsia isabellae, a rare and protected species in France, was slowed down and the pupal weight reduced. Also Thaumetopoea pityocampa was negatively effected through slower larval development and increased larval mortality. Thus, it has already been demonstrated that resistant clones of pine can have negative effects on non-target insects.

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The main methodologies to be used by the geneticist in order to improve forest tree resistance are first the search for useful genotypes, directly by screening tree provenances or clones or indirectly by using resistance markers. The next step is the use of those genotypes in genetic improvement programs. 4.1 SEARCH FOR USEFUL GENOTYPES The first step is the search for useful genotypes. To find them the existing genetic variability of trees and aggressors must be investigated. This is done generally by exposing clones to natural pest infection as seen in the results presented above. However, this method raises problems because there is no control of the variability of the aggressors, or of the level and homogeneity of the attacks (Doudrick et al., 1996). According to Bastien (1999), the lack of any control of the aggressor variability is the reason why clonal selection for poplar genotypes resistant to the rust Melampsora larici-populina turned out to be ineffective 10 years later. Another possibility is to perform laboratory tests which allow control over the aggressiveness or pathogenicity of the pest species, the attack level and the environmental conditions. In this situation however, the number of genotypes and the size of the experimental design is necessarily limited by the capacities of the laboratory. Also, due to the artificial environment of the experiment, results may not be replicable in the field. The use of markers linked to the tree response to aggressors is an important tool in the search for resistant genotypes. The important thing is that such indicators, whether or not involved in a causal relationship with tree resistance to the aggressors, must be correlated with the host response and resistance level. They can be biochemical, morphological, physiological or genetic indicators. 4.1.1 Biochemical indicators Several defensive chemicals (secondary metabolites) involved in the tree response to biotic aggressors have been proposed as biochemical markers (Bastien, 1999). Some have been proved to be related to tree resistance and can therefore be used as indicators of tree resistance to describe or to search for genetic diversity within the host population. They are summarized in Table 2. The phenolic composition of the wound resin of Scots pine (Pinus sylvestris) attacked by Leptographium wingfieldii, a fungus vectored by Tomicus piniperda, is very likely a chemical marker for resistance, since Bois & Lieutier (1997) found that high concentrations of taxifolin glucoside in unwounded phloem, and high concentrations of taxifolin, pinocembrin, pinosylvin and pinosylvin monomethylether in the reaction zone of wounded phloem could only be found in the resistant clones. It was also found that a high concentration of p-coumaric acid in the reaction zone could be an indicator of Scots pine susceptibility. Similarly, there is a highly significant correlation between ranking clones of Norway spruce (Picea abies) according to the general phenolic composition of their phloem and ranking them according to their level of resistance to artificial mass

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inoculation by Ceratocystis polonica, a fungus vectored by Ips typographus (Brignolas et al., 1998). This suggests that the phloem phenolic content could be used to predict Picea abies resistance to attack by Ips typographus and its associated fungus. This is also true for some particular phenolic compounds such as isorharpontin and catechin. The same authors found that the concentration of (+)catechin, 6 days after inoculation with the fungus, was higher in the resistant clones and that isoharpontin concentration was high in the unwounded phloem of the susceptible clones before any aggression. In another investigation Brignolas et al. (1995) found that resistant clones of Picea abies contained taxifolin and lower concentrations of piceid and isoharpontin and showed a higher tanning ability than those susceptible to C. polonica attack. As isoharpontin and taxifolin glucoside can be measured in unmanipulated phloem, they are valuable markers of tree susceptibility and resistance respectively. Christiansen et al. (1987) have suggested that the most critical variable to determine is the actual flux of carbohydrates involved in the synthesis of defense chemicals. However, no attempt has been undertaken yet to try to correlate such parameters with tree resistance. Instead, a recent study focused on a predominant role of the local reserves of the tree (Guérard et al., 2000). Indicators of resistance can also be found in other systems apart from conifers and bark beetles. Charles (1976) compared the resistance of different pine species to Rhyacionia buoliana. Pinus halepensis and P. pinaster were more resistant than Pinus contorta and P. ponderosa, which was attributed to differences in the terpene profiles. Intra-specific differences in terpene composition (phellandrene, 3-carene, camphene) have also been reported (Charles et al. 1982). The terpene 3-carene was found besides terpinolene in varieties of Pinus sylvestris resistant to Hylobius abietis attacks (Wright 1976). Jactel et al. (1999) found that the resistance of Pinus pinaster to Dioryctria sylvestrella was genetically determined and that terpinolene could be used to select susceptible genotypes. When testing biochemical indicators of resistance, it is however crucial to take into account possible physiological variations in the biochemical content of tree tissues. Auger et al. (1994) showed that taxifolin and taxifolin glucoside concentrations in Scots pine needles change with season. Taxifolin concentration peaks in autumn when taxifolin glucoside concentration drops. Taxifolin glucoside reaches its highest level from June to August when attacks by the sawfly Diprion pini take place. Seasonal changes in phenolics have also been observed in Q. petraea by Beres (1984). Moreover, within the same plant, differences in concentration can occur as leaves in the shaded part of the crown contained lower levels of taxifolin and taxifolin glucoside than leaves in the sunny part of the crown. Variations between populations can also make the use of resistance indicators difficult, as for the interaction between Pinus pinaster and Dioryctria silvestrella. In tree populations of Southeastern France, Sueron (1982) found a significant correlation between the terpene profile in bark tissues and resistance to the insect, but no correlation was found in Corsica. Due to such high physiological variations between individual trees and under different environmental conditions, the value of biochemical indicators of resistance is often very low. This however may depend on

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the chemical family. Until now, no difference in the phenolic content of Scots pine phloem could be found after severe experimental water stress, which tends to prove that phenolics do not vary much with the tree physiological status of the tree (Croise et al.,

1998). On the other hand, Chiron et al. (2000) observed that ozone pollution induces a hypersensitive phenolic response in the tree similar to that induced by fungus inoculations. Since there is no specificity in the tree response this might also be the case for the markers, and phenolics might thus be indicators of resistance to a high diversity of abiotic and biotic factors.

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4.1.2 Morphological and physiological indicators In addition to biochemical resistance markers, morphological and physiological parameters can also be used. In bark beetles the length of beetle galleries or speed of fungus extension in the phloem or the sapwood can be linked to tree resistance. In Scots pine, both parameters were larger in clones susceptible to mass inoculation with Leptographium wingfieldii than in resistant clones (Bois & Lieutier, 2000). Physiological indicators of tree resistance to bark beetles could also be tree productivity indices calculated as the ratio between wood production and leaf area (tree vigor index). Such indices have been demonstrated to be related to the threshold of attack density above which trees are overcome by natural attacks (Waring & Pitman, 1983; Mullock & Christiansen, 1986). High tree vigor indices were never found together with high content of phenolics, which fits with the growth-differentiation-balance hypothesis (Viiri et al., 1999). Other structural indicators of resistance to bark beetles could take into account the polyphenolic parenchyma cells of the phloem. These cells are active in the synthesis, modification and storage of phenolic compounds and are involved in constitutive and induced resistance (Franceschi et al., 1998). They have been reported to be 40% more frequent in P. abies clones resistant to artificial mass inoculations with C. polonica than in susceptible clones (Franceschi et al., 1998). A positive relationship exists between the freezing point of Picea sitchensis needles and the mortality of Elatobium abietinum. Thus the freezing temperature of the needles could be used as an indicator of the spruce resistance to the aphid (Parry, 1982). 4.1.3 Genetic markers Recently, genetic markers have been found by Hertel & Kaetzel (1999) for resistance of P. abies to the aphid Adelges laricis. The NADH-dehydrogenase B locus was investigated and it was found that homozygotes with a special isoenzyme (B1B1) were susceptible to the aphid, while homozygote genotypes with the isoenzyme (B2B2) were almost completely resistant. This does not mean that this enzyme influences resistance, but that other genes in the same linkage group might be involved. With the phosphoglucose-isomerase (Pgi B) locus, another genetic marker was found for the resistance to the sawfly Pristiphora abietina. Picea abies clones with the homozygote genotype (B3B3) contained much more carbohydrate than the heterozygote clones. All strongly infested clones had low concentrations of soluble carbohydrates and high chlorophyll concentrations, while clones with high soluble carbohydrate levels and low chlorophyll concentrations were less severely infested (Hertel & Kaetzel, 1999). In Pinus eliotti, Davies et al. (1999) identified a gene that codes for chitinase, an enzyme involved in many defensive processes. 4.2 GENETIC IMPROVEMENT PROGRAMS Genetic improvement of forest trees can be undertaken in three different ways: classical tree breeding, hybridization and genetic engineering. Genetic engineering

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and hybridization are of particular advantage because they achieve faster results than classical breeding programs. The new methods of genetic engineering are now available for the enhancement of resistance in forest trees and could be very useful. In agriculture it has already been introduced, and genetically engineered crops are becoming more and more important in several countries while other countries are opposed to their utilization. Transgenic forest plantations will likely have an important role to play in high intensity tree farming systems. Because of the limited history of forest tree domestication and the slow rate of traditional breeding programs imposed by long generation times, forestry is likely to benefit more from biotechnology than annual crops (IUFRO Working Party S2.04.06, 1999). An overview of the successful genetic transformation in trees was given by Levée et al. (1997). With the aid of Agrobacterium, genetic information can be introduced into the plant. For the first time, this was achieved for conifers by Shin et al. (1994), who inserted genes coding for herbicide resistance (aro-A-gene) and for insect resistance (Bt-toxin-gene) into larch (Larix decidua). The gene that codes for the toxin of Bacillus thuringensis has also already been introduced into poplars: Populus nigra in China to reduce damage from L. dispar attacks and Populus alba experimentally in France against attacks by Melasoma populi (Wang et. al. 1996, Ewald 1997). Also, the first introduction of that gene into the larch hybrids decidua X kaempferi was recently achieved (Ewald et al., 1999). However, using this technique in the field creates a permanent selection pressure for resistance to Bt, leading to rapid selection for resistant insect populations. According to Ewald (1997), this can be avoided by always planting genetically unmanipulated trees mixed with transgenic trees. Even more than one resistance gene should be offered to avoid the development of Bt-resistance in the insect populations. Problems also can arise regarding the low specificy of Bt. Indeed, the toxin acts on different kinds of insects, but lepidopteran species are especially susceptible, without any particular specificity. The presence of the toxin in the environment of insects all year round is thus critical from the view point of biodiversity. Populations of rare and endangered insect species can be further reduced or become extinct, since there is no way for them to avoid being in contact with the toxin. To reduce the effects on non target species, Ewald (1997) proposes to include promotors that turn on Bt-toxin only after attack, but such a promotor still needs to be found. Another critical point is the uncontrolled spread of transgenic material; Ewald (1997) argued that additional genes must be introduced into the plants leading to male sterility. But the author also states that, up to now, a stable genetic expression of that gene has not been achieved. 5.

ENHANCEMENT OF RESISTANCE BY SILVICULTURAL MEANS

Silvicultural enhancement of resistance is increasing the defence efficiency of any given tree genotype to the maximum level of resistance of that individual tree. This could be done by providing optimal environmental conditions for each tree species, because in most cases a tree that suffers from environmental stress has a lower level

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of resistance. Plants under stress can be a better food resource than unstressed plants (Plant Quality Hypothesis). According to Björkman & Larsson (1999) they have a higher nutritional value due to a higher content of soluble nitrogen and/or reduced resistance, because they produce less defence chemicals. According to Christiansen et al. (1987), every factor influencing crown size or photosynthetic activity in a negative way can reduce the level of defence chemicals and therefore increase susceptibility of a tree. This is in agreement with the GrowthDifferentiation-Balance-Theory (GDB); The production of defence chemicals is described as a trade off with growth (Herms & Mattson, 1992). Nutrient availability also influences defence levels, which is described in the Carbon-Nutrient-BalanceTheory (CNB); growth is the primary sink for assimilates during conditions favorable for growth, characterized by high nutrient availability (Tuomi et al., 1988). When conditions limit growth, differentiation and therefore the production of defence chemicals becomes the primary sink. The level of environmental stress can also influence resistance. A reduction in the stress levels on trees can create a pseudo-resistance against the insect pest (Bogenschütz & König, 1976), but the effects of moderate and severe stress may be different (Plant-Quality-Hypothesis). In all situations however, one must keep in mind that, if a silvicultural practice reduces damage, it is often difficult to determine if that is due to an increase in tree resistance or to an effect on the pest population itself or their natural enemies. There are several silvicultural practices that can influence tree resistance to insects: 1. stand compositions that fit the environment (natural vegetation); 2. plant trees only on sites that fit their ecological demands (moisture and soil conditions); 3. fertilization; 4. irrigation; 5. avoiding monocultures; 6. avoiding clean forestry; and 7. thinning (reduction of intra-specific competition). We explain these possibilities in the following sections, using GDB- and CND- Theory where appropriate, and using examples from research on European insects. 5.1 STAND COMPOSITION ACCORDING TO NATURAL VEGETATION Most stands that are severely attacked by forest pests in Central Europe are not growing within their natural distribution range, such as Norway spruce, which does not belong to the natural vegetation of Central Europe, except at higher altitudes as in the Bavarian forest or in the Alps. This situation enhances susceptibility to certain pests in different ways. For example, the climatic effects can act directly on the tree, such as the greater danger of drought in the lowlands, but climate can also have indirect effects by speeding up the development of the pests when the tree is growing under warmer than normal conditions (Merker & Müller, 1951; Merker, 1956; Kalandra, 1962; Vité et al., 1984). Severe bark beetle outbreaks in Central Europe very likely result from human actions leading to the production of two beetle generations per year (Schimitschek, 1953, 1954). In Western and Central Europe the cultivation of tree species belonging to potential natural vegetation is gaining more and more attention space in silviculture. In this context natural propagation of the trees is of advantage compared with planting, because natural genetic diversity is preserved.

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5.2 OPTIMIZATION OF SOIL PARAMETERS Soil conditions, especially soil water potential and nutrient content which depends on soil acidity (pH), play a major role in determining the distribution of tree species and genotypes in natural forest ecosystems (Ellenberg, 1996), and also the level of tree resistance. Viiri et al. (1999) state that unfavorable sites and climate conditions often reduce assimilation rates of plants and therefore can reduce their ability to defend themselves. This is also described by Führer (1975) as the resistance of a individual tree is not static but fluctuates, which is also true for resistant genotypes. Causes of such fluctuations are weather effects in combination with soil parameters. Therefore, resistance can also be enhanced by choosing the tree species and ecotypes that fit best with the site conditions (Schimitschek, 1969). In forestry however, this is only possible in a restricted way because the plant-insect-site relationships are still poorly understood. 5.3

FERTILIZATION

Bogenschütz & König (1976) give an overview of the effects that fertilization can have on different insect groups. According to several authors, fertilization of forest stands can increase resistance to disturbances in stands growing in unsuitable site conditions (Schwenke, 1960; Büttner, 1961; Merker, 1962). However, as practical experiences and causal analytic studies have shown (Luterek, 1969; Otto, 1970, 1971), the effect of this method is still very unsure. Only the exact evaluation of all processes involved can clarify the outcome of forest fertilization (Bombosch, 1972; Eidmann, 1963; Schimitschek, 1969; Thalenhorst, 1972). Contradictionary results could depend on different site conditions in the experiments and could be explained by the CNB-Theory. If site quality is already good, which means high nutrient availability, additional fertilization leads to higher growth activity and therefore the carbohydrate pool is depleted, and as a consequence resistance level sinks. On poor stands the additional amount of nutrients might not be enough to provide optimal conditions for growth, and therefore carbohydrate flow into growth is low and they stay available for defense. Hättenschwiler & Schaffelner (1999) reported increased performance of Lymantria monacha on Picea abies fertilized with N. In the fertilizer treatment, the concentration of starch, condensed tannins and total phenolics decreased, whereas sugar and N-concentrations increased, in agreement with both Plant-QualityHypothesis and CNB-Theory. Fertilization can also increase damage by sap sucking insect species, especially aphids. Viiri et al. (1999) investigated the influence of Nfertilization on resin flow and phenolics in P. abies and P. sylvestris. In Picea abies fertilization treatments increased tree growth, stem diameter and tree vigor index. This growth response was not reflected in resin flow and phloem phenolic content; in individual trees a combination of high tree vigor index and high phenolics / resin content was never found. This may be due to morphological barriers and / or resource based trade offs in accordance with the CNB-Theory. Nitrogen fertilization can increase the resin acid concentration in the needles formed one year after the

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fertilization treatment but not in the needles formed before treatment (Björkman et al., 1998), suggesting that the effects on defoliators may be complex. Kytö et. al. (1998, 1999) and Viiri et al. (1999) investigated the influence of nitrogenfertilization on the constitutive induced defence mechanisms of P. abies and P. sylvestris against attacks by bark beetles and their associated fungi. The fertilization treatment increased tree growth, stem diameter and tree vigor index. No effect was observed on resin flow and density of vertical resin ducts, parameters representative of constitutive resistance, and on phloem phenolic content in the reaction induced by fungus inoculations. The hypothesis that nitrogen fertilization reduces resistance could not be proved. Later however, on Norway spruce, it was found that nitrogenfertilization significantly reduced the concentrations of total stilbene aglycon and total terpenes in the phloem reaction zone induced by artificial inoculations with Ophiostoma polonicum, suggesting the tree’s ability to defend itself against aggressions was also reduced (Viiri et al., 2001). The entomological aspect of fertilization represents a step towards stabilization of food quality for the insects. This together with natural enemies could lead to stabilization of pest population levels (Bogenschütz & König, 1976). Enhanced resistance via fertilization is currently being tried by fertilizing susceptible spruce stands, but this must be undertaken with care because influences on the soil fauna are not yet sufficiently investigated. In this context, Funke (1990) showed, that after the use of calcium fertilizer in areas of Germany where soils depleted due to acid rain, drastical changes in soil fauna occurred. Therefore the effects of fertilization, not only on the resistance of forest trees but on the whole ecosystem, must be investigated carefully before it is applied over a large range. Also vast areas of landscape, that had so far been unfertilized will disappear and the whole area will sooner or later be covered only with eutrophic ecosystems. This will increase pressure on many plant species requiring oligo- and mesotrophic conditions, and thus species extinction will be enhanced. 5.4 IRRIGATION Christiansen et al. (1987) state that water stress increases host tree susceptibility by affecting the exudation of resin so that bark beetle colonization is easier. The content and production of monoterpenes can be influenced by water stress; the stronger the water stress, the more monoterpenes are released (Mattson & Haak, 1987). Bark beetles may take advantage of this, because they are able to identify susceptible trees by a high level of monoterpenes in the odor plume around them (Baier et al. 1999). In accordance to the GDB-Theory, Lorio & Hodges (1968) and Christiansen et al. (1987) point out that moderate water stress (short term drought) does not stop photosynthesis completely and therefore carbohydrate reserves would be even larger, because shoot growth requires less carbohydrates during drought. The tree can therefore become even more resistant under moderate drought (Christiansen & Glosli, 1996). On the other hand, long term extended drought would stop photosynthesis completely and the carbohydrates would thus be depleted, leading lowered production of defense chemicals. This could be an explanation for the severe bark beetle outbreaks that are often observed after long drought periods.

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Moderate stress can be defined as a situation where the relative extractable water in the soil is not less than 40% of the water reserves (Granier et al., 1999). Under these conditions, in the temperate zones of Western and Northern Europe, only moderate stress occurs in nature. In Central Europe, an acute drought can occur, mostly restricted to late summer and fall. This does not cause problems in Northern countries, but in Central and Western Europe this is just the time when the first beetle generation starts colonization of new trees, therefore allowing the insects to take advantage of the drought. Furthermore, drought is expected to have a stress effect of decreasing magnitude upon sucking, mining, chewing and gall forming insect species (Larsson, 1989). However, results on Picea abies do not fit completely with the plant stress insect performance hypothesis (Björkman & Larsson, 1999). Mining insects (Epinotia tedella) were more sensitive than expected to changes induced by drought stress in their host plant, and the response of galling insects (Sacchiphantes abietis) needs to be divided into at least two different aspects: gall occurrence and size. Drought had a positive effect on gall initiation but a negative effect on gall growth. Nevertheless, drought had no effect on the chewing sawfly (Gilpinia hercynae) where as larger numbers of sucking aphids with wing buds were observed on drought stressed trees; which is in accordance with the original hypothesis. For practical use irrigation is not a very suitable way to manipulate tree resistance. There are high technical demands in the construction and operation of irrigation systems and limited availability of water or competition for water use with agriculture. 5.5

AVOIDING MONOCULTURES AND CLEAN FORESTRY

Clean forestry, where any dead wood is removed from the stands, decreases the possibilities for natural enemies to survive because their prey or hosts are kept at very low population levels. Together with monoculture, this situation can enhance the chance of mass outbreaks of the pest species after windfall or severe drought. In monospecific forests, bark beetles at low endemic population levels before windfall can breed in low densities in the highly susceptible damaged trees which increases their performance. Their populations can then easily reach the epidemic stage during which healthy trees can be killed by mass attacks (Thalenhorst, 1958). Nevertheless, there are also several cases where monocultures do not increase damage and other cases of important damage in mixed forests. The problem is not clear and further research in this field is required. In many European forests, there are always some very weakened or recently felled trees that stay in the forest. In contrast, in Southern China absolutely no wood stays in the forest because it is immediately collected by local people for firewood. This lack of trees without resistance may be the reason why Tomicus piniperda massively attacks shoots in Southern China at the end of the winter (100% of the shoots can be killed). This massive shoot attack induces such a dramatic reduction in tree resistance that the trunk attacks succeed and trees are then killed by the beetles (Ye & Lieutier, 1997).

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In Europe T. piniperda rarely kills trees, possibly because it always find some suitable breeding material on the ground. 5.6 THINNING Thinning reduces intraspecific competition between trees and therefore can also be used to reduce the stress level of a plant and increase access to water, nutrients and light. This allows higher photosynthetic rates and more carbohydrates are thus available for growth and defense. Indeed, several authors found a relationship between bark beetle attack level and indicators of severe competition, such as reduction in radial growth (Hard, 1985) or crown competition (McCambridge & Stevens, 1982; Worell, 1983a,b). For defoliators, a beneficial effect of thinning was also reported, as found by Habermann & Bester (1997) for L. monacha on Pinus sylvestris. But thinning can enhance bark beetle attacks because of root damage, resulting from an increase in air turbulence in the stand (Christiansen et al., 1987). 5.7 OTHER PARAMETERS Complications in the use of silvicultural practice arise because a combination of various factors can interfere. Lunderstädt (1999) found that infestation of F. sylvatica stands by Cryptococcus fagisuga is promoted by combinations of the following factors: accelerated flushing in cool, unthinned valley sites and reduced flushing on warm, thinned plateau sites. In the case of both extremes the resistance was lower. It must also be mentioned that, in certain areas of Central Europe, air pollution with also plays a role in insect damage, reducing tree resistance and leading to severe outbreaks especially of bark beetles (Scherzinger, 1996). The effects of can also be explained by GDB- and CNB-Theories. Thus, air cleaning measures also are a potential tool to enhance resistance of forest stands. Man-made accumulation of in the atmosphere could have an influence on plant resistance. Such effects have been reported by Hättenschwiller & Schaffelner (1999) on the performance of L. monacha larvae on P. abies. In assays under high concentration, larvae reached 35% less biomass compared to the experiment under ambient concentrations. In high treatments, specific leaf area and N content were decreasing but concentrations of starch, condensed tannins and total phenolics increased. 6. PROSPECTS AND CONCLUSIONS Increased resistance of forests to insect pests could be achieved by several means, but the details of how this can be accomplished are not completely understood. Many investigations about differences in susceptibility of clones and provenances of forest trees to insect attacks have been undertaken up to now, but the mechanisms of inheritance are still poorly understood (Lévieux, 1986), mainly because of the influence of the environment which can lead to pseudo-resistance. To clarify this

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point, it is necessary to segregate genetic from pseudo-resistance in controlled laboratory experiments. In this context Bastien (1999) pointed out that it is important to know how a variable environment can change resistance performance of the genotype, since this genotype-environment interaction might limit tree resistance in time and space. Therefore especially variable climatic conditions, such as extreme drought must be evaluated experimentally as well. Because of the intense pressure from numerous pests, maintaining genetic variability in forest tree populations is a necessity. In addition, a sufficient level of genetic variability is considered as a prerequisite for long-term stabilization of hostparasite interactions because of pre-adaptations and redundancy in ecosystems (Hertel & Kaetzel, 1999). Parallel to the study of host variability in resistance, it is also important to take a close look at the genetic diversity of the pest insects and the pathogens vectored by them, especially to take into account the adaptive capacity of the pests to host resistance. In Europe, that has already been done for T. viridiana (Du Merle, 1988) and presently this topic is an important aspect of forest entomology research. It concerns a wide array of pest guilds, such as sap sucking, defoliating, cone and seed insects, and bark beetles and their associated pathogenic fungi. The reactions of natural enemies to improve of tree resistance are also an important aspect that must be investigated carefully. Indeed, when the plant resistance level against the pest is increased by any method, population density of the pest is lowered, and this may cause problems for the complex of natural enemies controlling the pest. Increased resistance might cause a food shortage for the third trophic level and therefore their regulative capacity could be lowered (Führer, 1975). This concern is even more relevant in intensely managed monocultures where the population densities of prey or hosts are very low during the endemic stage of the population dynamics and therefore populations of natural enemies are already limited in their ability to increase. Raising resistance of such stands will even more diminish the regulatory effects of the antagonistic complex. Therefore it is crucial that a critical level of the prey population density is maintained. In most cases it is not yet known, how high the critical prey or host population must be to sustain population of natural enemies. It has thus been proposed to avoid the use of resistance enhancing measures in areas with low bark beetle population densities (Führer, 1975). Moreover, as pointed out by Führer (1975), all forest practices at the moment try to reduce food quality for the pest insects to raise their mortality. Due to this, the risk of gradation increases because many pests such as Bupalus piniarius are mainly controlled by natural enemies, which are reduced in density due to food shortage when their prey populations are reduced below a critical threshold. Instead of cultivating resistant genotypes, it seems more advantageous to stabilize food quality, and therefore also the stage of susceptibility in combination with augmentation of natural antagonists. It is thought that the antagonists can influence pest populations more, if plant attributes which are important for pest population development only show low oscillations under extreme environmental conditions. Paine et al. (1993) also state that high tree vigor and growth can be reached by

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CHAPTER 12 DEPLOYMENT OF TREE RESISTANCE TO PESTS IN ASIA

NAOTO KAMATA

Kanazawa University, Kakuma, Kanazawa, Ishikawa 920-1192, JAPAN

1. INTRODUCTION

1.1 TREE BREEDING IN CHINA In China, the total land area is with of forested area. The percentage of forest coverage is ca. 13% of the total land area. After 1950, ca. 4.5 million ha of land was planted every year. In 1987, the total area of artificial forests was 28 million ha. The main purpose of tree breeding from the 1950s to the early 1980s has been to breed fast-growing trees to re-establish vegetation on degraded land (Gu 1987). The influence of Lysenkoism (the belief that plants could acquire genetically improved traits by growing them in new environments) slowed the progress of tree breeding by the 1960s. At the early stage, selection had been the main method of tree breeding. During later periods, breeding by crossing and hybridization of poplars were the major projects. Thereafter, hybridization of pines (Pinus spp.), willows (Salix spp.), and larches (Larix spp.) also started. The major governing ideas of the tree breeding were heterosis, genetic additivity, and genetic complementation. Because fast-growing trees tend to be infested by pests, many plantations of poplars and willows are susceptible to attack by insects. Pest of fastgrowing plantations include: longhorn beetles, Apriona japonica, Batocera lineolata, and B. horsfieldi, and folivorous insects, Lymantria dispar and Apocheimia cinerarius. Projects to breed insect-resistant tress have been going on since the 1980s (e.g. Zhu and Zhang 1991; Wang 1995). One of the major projects 265

M.R. Wagner et al. (eds.), Mechanisms and Deployment of Resistance in Trees to Insects, 265–285. © 2002 Kluwer Academic Publishers. Printed in the Netherlands.

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has been the development of transgenic poplars transformed with the Bacillus thuringiensis toxin gene. A major project is the selection and breeding of super poplar clones for fibre production that are resistant to wood-boring insects. 1.2 TREE BREEDING IN SOUTH KOREA In South Korea, a forest rehabilitation program started after the Korean War. The major trees planted for rehabilitation have been pines and poplars (Shim 1987). Breeding of popular started in 1953. In 1954, more than 300 strains of Italian cultivars of poplar were introduced. Amongst these, the cultivars, I-214, I-476, and V-211, were selected as cultivars suitable for the climate in Korea and were planted in areas totalling ca. 670,000 ha. The hybrid, P. alba X P. grandulosa was thought to have the best of both parents and has been planted in an area totalling ca. 180,000 ha since 1967. The F1 progeny grew fast but were highly susceptible to the salty air from the sea. In the late 1950s and early 1960s, a great amount of Pinus taeda pollen was introduced from the USA to breed the hybrid Pinus rigida X P. taeda (P. rigitaeda). Because P. rigi-taeda grew 2.5 times faster than P. rigida when it was young, ca. 1,000 ha of plantations were established. However, this hybrid was not tolerant to strong cold wind in winter and the growth rate slowed down as it matured. Many native pine trees have also been planted but have been damaged badly by the pine needle gall midge, Thecodiplosis japonicus. The Korean Forest Research Institute first tried to select a resistant strain but changed the strategy to breed hybrids by crossing between susceptible and resistant species (Son et al. 1999). Effective hybrids of insect-resistant pines were obtained using this technique. Pine wilt disease caused by the pinewood nematode (PWN), Bursaphelenchus xylophilus, is also a serious problem in the southern part of South Korea (La et al. 1999). An experiment to test the cold tolerance of the hybrid, P. thunbergii X P. massoniana, is in progress (Shim 1987). 1.3

PEST-RESISTANT TREE BREEDING IN JAPAN

In Japan, breeding larch trees resistant to the vole, Clethrionomys rufocanus, has been successful. As for pines, selection for P. thunbergii clones that are resistant to T. japonensis is the most successful and advanced among many projects in Japan. DNA markers available for marker-assisted selection (MAS) of resistant trees have been identified. The pine wilt disease caused by pinewood nematode has been the most serious pest for the past 30 years. A national project to select pine trees that were resistant to PWN started in 1978, which was successful for P. densiflora and P. thunbergii. The hybridization of P. thunbergii X P. massoniana also started in 1983. These resistant pines have started to be used in plantations. As for the Japanese cedar, Cryptomeria japonica, selections for clones resistant to each of several barkand wood-boring insects have been carried out (Tajima 1990, Tamura et al. 1996, Ueki 1999).

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2. POPLAR 2.1 BREEDING OF POPLARS IN CHINA Poplars are distributed almost throughout China. They include 59 species, 35 varieties, and 11 cultivars. In China, hybridization of poplars has been conducted since the 1960s. Some of the major parent tree species were P. simonii, P. nigra, P. cathayana, P. alba, and P. pyramidalis. Hundreds of hybrids were tested each year. Table 1 shows the major popular cultivars that were developed in the 1960s and that have been planted in the country. The major goals of the poplar breeding program were to develop cold-tolerant, fast-growing trees for the northern regions and to develop fast-growing trees in the regions around the Chang Jiang River, in central China.

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2.2 TRANSGENIC POPLAR PLANTS TRANSFORMED WITH THE BT TOXIN GENE IN CHINA In China, transgenic poplars, Populus nigra and P. deltoides, transformed with the Bt toxin gene have been developed to protect them from insect defoliation (Chen et al. 1995a; Tian et al. 1995). An effective regeneration system for P. deltoides was first developed by Chen et al. (1995a). Agrobacterium tumefaciens LBA 4404 strains harbouring the Bt toxin gene expression vector pB48.214 or pB48.215 were used for transforming poplar plants by means of the leaf disc method. After transformation, adventitious buds formed at the cut explant on media with kanamycin nearly one month later. When shoots reached 1cm long, they were transferred to rooting media and supplemented with kanamycin. PCR analysis showed that Bt toxin genes were successfully integrated into the P. deltoides chromosomes. A similar regeneration system was developed for P. nigra (Tian et al. 1995). Transformation of P. nigra was obtained by co-cultivating leaves and stem segments with A. tumefaciens LBA 4404 carrying the binary vector containing the toxin chimeric gene. Candidates of transgenic plants were selected from regenerated Kanamycin-resistant plants by DNA-DNA hybridization. Insect tolerance tests proved that the transgenic plants were toxic to two defoliating insects, Lymantria dispar (Lepidoptera: Lymantriidae) and Apochima cinerarius (Lepidoptera: Geometridae). Transgenic plants were selected based on the Southern blot of the PCR products and a cluster analysis using the trees’ growth and insect resistance (Tian et al. 1995). The western blot analysis showed that the Bt toxin gene was not only inserted into the chromosomes of poplar but also was expressed into protein, which explains the high insect resistance of these plants (Cheng et al. 1995b). 2.3. SUPER POPLAR CLONES RESISTANT TO WOOD-BORING LONGHORN BEETLES The cultivars I-63, I-69, and I-72 were introduced to China in 1972 from Europe and have been planted in Hua Dong (East of China) and Hua Zhong (Centre of China) (Table 1). However, these were sometimes heavily infested with longhorn beetles and many trees died. In Hubei Province, Cao et al. (2000) investigated insect damage by A. japonica and B. lineolata to these three major introduced poplar cultivars planted in three disjunct locations. The authors found a significant effect of location on the insect damage. However, no consistent relationship was found between the amount of damage and the tree cultivar. The selection and breeding of super poplar clones as fibre products that are resistant to a wood-boring longhorn beetle, Batocera horsfieldi, has been conducted in China since 1983 (Qing 1991). Artificially controlled pollination was conducted in 1983 using I-69 as the female parent plant, and using P. nigra, I-63 and P. x euramericana (Dode) Guineir. cv. “Seroutina 272” as the male parent plants. Cross combinations were numbered No. 32 for I-69 X P. nigra, No .34 for I-69 X I-63, and No. 37 for I-69 X P. x euramericana. A field test to compare the hybrid clones was carried out in Mian

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County, Shangxi Province, after selection in the nursery (Wang et al. 1995). At first, 23 clones including two control clones were tested. These 23 clones were divided into three groups by using a systematic cluster analysis. The first group (G1) included trees that were fast-growing and that had a high resistance to B. horsfieldi. This group included the clones 34-37, 34-135 and 34-314. The second group (G2) included clones that grew fast but that were less resistant to B. horsfieldi. This group included I-69 and 12 hybrid clones including 34-301. The third group (G3) included trees that grew slowly and that were less resistant to B. horsfieldi. This group included all the clones originating from combinations of No.32 and No.37, and P. x euramericana (control). The resistance of G1 was significantly higher than the resistances of G2 and G3. Based on their high resistance (100%), clones 34-37 and 34-135 were combined to form a subgroup named Nan-Kang No.l. Clone 34-314, which was slightly damaged by B. horsfieldi, was named Nan-Kang No.2. Second, two poplar clones (34-301 and 34-286), which grow fast, are resistant to insects, and have good quality, were selected. Nine years after planting, Clones 34-301 and 34286 were 24.9% and 16.6% higher than that of I-69, respectively, and 16.7% and 8.9% higher than that of 34-314 (Nan-Kang No.2), respectively. Clones 34-301 and 34-286 were significantly more resistant to B. horsfieldi than I-69: the number of B. horsfieldi per tree was 0.4 for 34-301, 0.5 for 34-286 and 5.38 for I-69. There was a positive correlation between the resistance to B. horsfieldi and the total phenolic contents. By a random amplified polymorphic DNA (RAPD) analysis, a molecular marker (OPAD-01) was found, which is linked to genes of resistance to B. horsfieldi and is useful for MAS of resistant trees (Wang et al. 1995). 3. PINE 3.1 PINE NEEDLE GALL MIDGE, THECODIPLOSIS JAPONENSIS The pine needle gall midge, T. japonensis, was first found in central Japan (Sasaki 1901). This insect forms a gall on the basal part of the needles. Heavily infested pine trees are weakened and sometimes die. Population outbreaks of this insect were recorded in 1929 in Korea (Takagi 1929). In Korea, more than 300,000 ha of pine plantations are heavily damaged by this insect every year (Office of Forestry Korea 1981). In Japan, the first outbreak record was reported around 1950 from Nagasaki Prefecture in Kyushu, the southernmost main island of Japan (Takizawa 1964). The outbreak area spread from the southwest to northeast (Sone 1986). In 1976, outbreaks were recorded in Hokkaido, the northernmost main island. An outline of the life history of T. japonensis in central Japan is as follows (Sone 1986). This species is univoltine. Adults emerge from the end of May to late June with a peak in mid-June. The life span of adults is about one day. Females copulate soon after emergence and deposit egg batches on the surface of the cavity between a pair of developing needles in a fascicle. The incubation period is about one week and newly hatched larvae move to the base of the needles where they form galls. The larvae moult two times in the galls, and matured third instars drop from galls to the ground during the period from November to March in the following year. The dropped larvae crawl into the litter layer and the surface of the soil, where most of

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them spin cocoons and over winter. Pupation takes place from April and adults start to emerge from the end of May. There is great variation in pine tree resistance to T. japonensis among species (Furuno and Sone 1978; Furuno 1987; Sone 1987) and also among individuals within the same species (Nishizawa 1969; Ozawa l971; Saito 1978). There are great variations in the number of deposited eggs among tree species and among individual trees of the same species. However, the number of eggs deposited did not have any significant relationship with tree resistance to T. japonensis (Terada 1992). Both among-species and within-species variation in the resistance are related to the mortality of hatched larvae after entering the needles. The salicylic acid concentration in the needles was closely related to the insect mortality (Son et al. 1999). Pine species highly resistant to T. japonensis contained higher concentrations of salicylic acid. For example, the salicylic acid concentration in needles of P. virginiana and P. rigida was 37 ppm to 50 ppm. However, as for P. thunbergii and P. densiflora the concentration was below 10 ppm. Salicylate-mediated signal transduction plays an important role in disease resistance (Klessig and Malamy 1994). A high concentration of salicylic acid induces expression of a stilbene synthase (STS) gene in pines (Kubota et al. 1996; Yamauchi et al. 1997). When salicylic acid was applied externally, the contents of internal salicylic acid in the needles of susceptible pines increased from 9.5 ppm to 20.6 ppm after direct external irrigation of salicylic acid solution and flour treatment on the roots. As a result, the frequency of gall formation decreased to a level that was 17-19 times lower than that of the control. In Korea, hybridisation has been the major strategy to breed resistant pines against T. japonensis. In Japan, a project to breed pine trees that are resistant to T. japonensis started in 1971 (Terada 1992). This project is considered as one of the most successful among many projects to breed trees that are resistant to pests in Japan. In order to develop P. thunbergii that are resistant to this insect, 60 candidate trees, which were growing without signs of damage in severely damaged maritime forests of P. thunbergii, were selected. Thirty-six of the selected trees were found to be free from the parasitism of T. japonensis following inspections. In further testing 9 of the 36 trees were attacked by T. japonensis at the same rate as damaged trees. A clonal test of the selected trees was carried out by planting grafted ramets as a block in the severely damaged forest and then leaving the planted materials under natural conditions. Thirty-eight clones out of the 53 tested had either zero or a very low percentage of parasitism. From the results of the inspection of the selected trees and their clonal test, 42 trees were judged to be resistant to the gall midge. In progenies produced from artificial pollination, the seedlings were segregated into ones with non-parasitism (0%: resistant) and ones with high-parasitism (81-100%). Seedlings with a parasitism percentage of 1-80% appeared very rarely. The average frequencies of appearance of resistant seedlings were 73% in the progenies of Resistant X Resistant, 48% in Resistant X Non-resistant and 0% in Non-resistant X Non-resistant, respectively. From the above segregation ratio, the resistance of the P. thunbergii to T. japonensis appears to be governed by one dominant gene and the parent trees used for pollination were heterozygous. Three RAPD markers linked to

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the resistance gene (RPGM) were detected by a bulked-segregate analysis (Kondo et al. 2000). Of these three markers, was also located in the confirmed map position in the map made by AFLP, and and were regarded as accessory markers at its most likely position (Hayashi et al. 2001). These markers might be useful for MAS of resistant trees. Hopefully, the function of the resistance gene (RPGM) will be investigated and the relationship between the function of this resistance gene (RPGM) and the salicylic acid concentration in the needles will be examined in future studies. The proximate factors causing the mortality of hatched larvae after entering the needles should also be studied. 3.2 PINE WILT DISEASE CAUSED BURSAPHELENCHUS XYLOPHILUS

BY

PINEWOOD

NEMATODE,

The major pine species in Japan, P. densiflora and P. thunbergii, have suffered heavy mortality for several decades (Kobayashi 1988; Kishi 1995). In the early 1970’s, the causal disease agent was found to be the pinewood nematode (PWN), B. xylophilus (Kiyohara and Tokushige 1971). The Japanese pine sawyer (JPS), Monochamus alternatus (Coleoptera: Cerambycidae) is the principle insect vector in Japan. The existence of the nematode was reported in the United States, where only exotic pine plantings were severely damaged suggesting that the nematode was native in the US. Recent genetic studies of the systematics of PWN found that PWN in Japan had possibly been introduced from the USA and that PWN in Asian countries was derived from the same strain (Iwahori et al. 1998). A large-scale national control project was started in 1977 when a federal law was passed complementing an insecticide spray program by either federal or local governments. The major control tactics were aerial spraying of standing trees to kill aerial populations of the vector insects and using the cut-and-treat method for treating infested logs to kill the vectors before emergence. The latter method includes cut-and-spray, cut-and-burn, and cut-and-slash methods. The resistance of pine trees to PWN varies greatly among tree species (Futai and Furuno 1979; Furuno 1982; Furuno and Futai 1986) (Table 2). At the species level, there is a close relationship between susceptibility and phylogenic classification: pine species belonging to the subsection Australes are the most resistant, followed by the subsection Contortae. Pines belonging to the subsections Ponderosae and Oocarpae are susceptible. The subsection Sylvestris contains both resistant and susceptible species. The resistance also has a relationship with geographical distribution (Furuno et al. 1993): the resistant pines (ranked HR and R in Table 2) are distributed in only two regions, the east coastal area of North America and the area from Taiwan- S China-southern part of Himalayan mountains.

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Pathophysiological changes during the development of symptoms of pine wilt disease is as follows (Fig. 1) (Fukuda 1997): The development of symptoms is divided into two stages: the early and advanced stages. In the early stage, a small number of nematodes migrate into the cortex, and then into the xylem of the stem, and induce denaturation and necrosis of parenchyma cells (Ishida et al. 1993), which result in terpene synthesis in xylem cells and embolism in tracheids. Such changes in the early stage can be induced in both susceptible and resistant pine species by either virulent or avirulent isolates of PWN. No change occurs in the physiological status of leaves, and nematode reproduction is suppressed during the early stage (Fukuda and Suzuki 1988a, b). Pine trees can survive if the symptoms do not progress from this stage. The symptoms of the advanced stage usually occur only in susceptible pines infected by virulent nematode isolates. At the beginning of the advanced stage, enhanced ethylene production by stems that coincides with cambial destruction occurs (Mamiya 1975, 1980, 1984, 1985; Mori and Inoue 1986) and results in embolism of the outermost xylem in the portion (Fukuda 1997). The embolism causes a decrease in leaf water potential and cessation of photosynthesis (Fukuda and Suzuki 1988a, b). After cessation of photosynthesis, symptoms develop drastically with a burst of the nematode population.

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Some of the secondary metabolic compounds in pine trees relate to pine wilt disease caused by PWN (Table 3). Resistance of pine trees to PWN must separately be discussed at each of at least two different stages of PWN infection: resistance at the time of PWN invasion into the bark and resistance in the wood after invasion. PWN has some difficulty in invading the bark of a resistant pine, P. taeda, but easily invades the bark of a susceptible pine, P. thunbergii (Futai 1985a, b) suggesting that the resistance of pine trees at the time of PWN invasion is related to a species-level difference in pine resistance to PWN. Unidentified water-soluble substances in pine bark were responsible for immobilization of PWN (Bentley et al. 1985) and acted as a repellent against PWN (Futai 1979). The quantity of the active substance from P. taeda was greater than that from P. densiflora (Bentley et al. 1985). These watersoluble substances were thought to act as a constitutive defence of pine trees at the time of invasion (Futai 1987). After a successful invasion, the nematodes increased in number and spread rapidly in the susceptible pine trees, but not in the highly resistant trees such as P. taeda. The responses of the resistant pine species, wound periderm formation and occlusion of cortical resin duct, trapped the nematode within

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damaged tissue (Ishida et al. 1993; Yamada and Ito 1993a). Since PWN never invaded the trunk, the tree survived although the inoculated branches died. Among secondary metabolic compounds shown in Table 3, pinosylvin monomethylether (PSME) showed the strongest virulence to PWN, which was followed by pinosylvin (PS). After PWN invasion, these stilbenes, PSME, PS, and 3-0-methyl-7,8dihydropinosylvin (MDPS), rapidly accumulated in the wood of the basal part of inoculated branches and the bark of the branches of P. strobes, which is ranked as “resistant” in Table 2 (Yamada and Ito 1993b; Yamada et al. 1999). These stilbenes act as an induced defence against PWN. However, in P. thunbergii, which is ranked as “highly susceptible”, no PS and PSME concentrations were recognized after inoculation of PWN (Yamada and Ito 1993b). For P. densiflora, stilbene synthesis was not induced by the infection of PWN (Yamada and Ito 1993b) although P. densiflora has the STS gene (Yamauchi et al. 1997). These facts indicate that PWN infection did not induce expression of the STS gene in P. densiflora.

In Japan, a national project to select resistant pine trees started in 1978. Survivorship of P. densiflora after PWN inoculation was 63.2% (37.9-84.6%) for the selected clones and 47.9% for non-selected clones (Toda 1999). Pinus thunbergii, which is an important species for protecting the seashore, is much more susceptible to PWN than P. densiflora. Survivorship of P. thunbergii after inoculation of PWN improved considerably from 12.5% for non-selected clones to 50.7% (29.1-67.9%) for the selected clones. Another way of breeding pines that are resistant to PWN is hybridization. The hybridization, P. thunbergii X P. massoniana, was first conducted in the USA in the 1930s (see Furukoshi 1986). In Japan, crossing of various combinations of many pine species have been tested since 1972, which proved the high compatibility between P. thunbergii and P. massoniana. An international hybridization project of P. thumbergii X P. massoniana was started in 1983 by introducing 20 liters/year of P. massoniana pollen from China. The same hybrid was also studied in Korea (Shim 1987). The

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tolerances of the hybrids to cold climate, strong winds, and sandy soils have been tested both in Korea and Japan. Trials of artificial hybridization between P. thunbergii X P. densiflora have also been conducted (e.g. Toda et al. 1990) because a natural hybrid between P. thunbergii and P. densiflora was found to show a stronger resistance to PWN than P. thunbergii (Ooyama and Shiraishi 1981). Several studies have reported that prior inoculation with an avirulent isolate of PWN induced resistance of young pine trees in the nursery and of adult pine trees in the forests (e.g. Kiyohara 1989). In the case of resistance-induced seedlings, embolism in the xylem was conspicuous, but water conduction was maintained in a very thin layer of the outermost xylem near the living cambium, and PWN did not multiply (Fukuda et al. 1997). Induced resistance of pine is considered as one of the possible control tactics of pine wilt disease (Kosaka 2000).

4. LARCH 4.1

LARCH IN HOKKAIDO, JAPAN

The Japanese larch, Larix leptolepsis, is the only native larch species in Japan. Natural distribution of Japanese larch is restricted to the high elevation areas in Central Japan. However, it has been widely planted in Europe, North America and Asia because it grows well in cold regions. Especially in Europe, the hybrid Dunkeld larch L. x eurolepsis (Larix decidua X L. leptolepsis) is one of the major plantation tree species because of its fast growth, good shape, and resistance to canker. In Japan, it is also widely planted in central and northern Japan, especially on the island of Hokkaido. However, L. leptolepsis tends to suffer serious damage by the vole Clethrionomys rufocanus, and many trees died by girdling. Larix gmelini var. japonica, which is naturally distributed in the Kuril Islands and Sakhalin, suffers little damage by the vole but it has not been planted in Hokkaido Island much because it grows slowly there. The hybrid L. g. var. japonica X L. leptolepsis has been widely planted because it suffers little damage by the vole and grows faster than L. g. var. japonica. Recent studies reported that there is a great variation in the vole resistance both in the hybrid and L. g. var. japonica (Nagata et al. 1989). The resistance of the hybrid was closely related to the resistance of their parents. Compounds that are repellent to the vole were identified as 13-epimanool and larixol (Sukeno and Ozawa 1997). Larixol showed activity at a concentration of 0.25%. The compound 13-epimanol showed activity at a concentration of 0.5%. These compounds will be useful tools for instant screening for vole resistance in larch trees.

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5. JAPANESE CEDAR, CRYPTOMERIA JAPONICA 5.1 HISTORY OF CRYPTOMERIA JAPONICA PLANTATION IN JAPAN The Japanese cedar, Cryptomeria japonica, is the major commercial conifer plantation species in Japan. The natural range of its distribution is Honshu, Shikoku, Kyushu, and Yakushima Islands. Pure native stands of Japanese cedar still remain in Yakushima Island and the west coastal area of the northeast part of Honshu Island. In Japan, after WWII, natural broad-leaved forests were cut over and changed to conifer plantations. Japanese cedar has been one of the major plantation species and is planted from the southern part of Hokkaido Island to Kyushu Island, which is wider than its natural distribution. In the Japanese cedar plantation, tussock moth Calliteara argentata (Lepidoptera: Lymantriidae) populations sometimes reach outbreak levels and cause serious defoliation. After insect defoliation, the mortality of Japanese cedar was reported to be 13.0-28.6% (Shibata 1981). Several wood- and bark-boring insects that reduce timber value have been considered as more important pests than C. argentata. These species include the bark borer Semanotus japonicus (Coleoptera: Cerambycidae), the twig borer Anaglyptus subfasciatus (Coleoptera: Cerambycidae), the bark midge Reeseliella odai (Diptera: Cecidomyiidae), and the bark moth Epinotia grantialis (Lepidoptera: Tortricidae). Improvement of Japanese cedar has been focused on to breeding trees that are resistant to these wood- and bark-boring insects except for A. subfasciatus, damage from this insect can be avoided completely if trees are pruned to remove dead branches. Pine trees have constitutive resin ducts, but Japanese cedar does not. Therefore, traumatic resin duct formation seems important to reduce damage by these insects. However, the mechanisms of resistance to each of these insects are different among insects and sometimes contradictory to each other. When larvae of E. grantialis were released into the trunks of the Japanese cedar that had been regarded to be highly resistant to S. japonicus, most of E. granitalis larvae grew to the adult stage contrary to prediction (Kato 2000). This result suggests that the resin flow from the inner bark, which was regarded to be most important to protect against attacks by S. japonicus larvae, could not protect against attacks by E. japonicus. Possible reasons for the difference in effectiveness of the resin flow are a difference in the boring period and a difference in the boring system between the two pests. Larvae of E. granitalis bore in early of the seasons when the host trees cannot metabolically respond to the attack. The boring period of E. granitalis is shorter because it ingests only a small amount of plant tissue. Because of its high mobility, E. granitalis larvae can escape from wood if the resin flow deters the course of boring. Because young larvae of E. granitalis start to feed on current-year shoots, the characteristics of current-year shoots are probably more important in determining tree resistance to E. granitalis. The thickness of inner bark is an important factor determining resistance of Japanese cedar both to S. japonicus and to R. odai. To make matters worse, trees with a thin inner bark are resistant to S. japonicus but more susceptible to R. odai (see below).

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5.2 BARK MIDGE, RESSELIELLA ODAI In the year 2000, the bark midge, R. odai, was distributed in Kyushu Island and in the westernmost part of Honshu Island, and is believed to be spreading eastward on Honshu Island (Sudo et al. 2000). In these areas, the damage caused by R. odai is serious for Japanese cedar forestry. When the larvae of this insect feed on Japanese cedar, timber values are reduced by stains in the sapwood. A project to breed Japanese cedar that is resistant to R. odai started in 1985. In this project, trees that were not infested by R. odai and those on which no stains were formed, although they were infested by this insect, were considered as “resistant” and have been selected (Tajima 1990). The mechanism of resistance is still unclear. However, resistance is closely related to the thickness of the inner bark. The stain is formed by the digestive fluid secreted by the larvae feeding on the surface of the inner bark. When the inner bark is thick enough to prevent the fluid from reaching the cambium, no stains were formed in the xylem although flecks were formed in the inner bark (Figure 2) (Yoshida and Sanui 1979). Therefore, Japanese cedar with thick inner bark is considered to be “resistant” to R. odai.

5.3 BARK BORER, SEMANOTUS JAPONICUS Semanotus japonicus (Coleoptera: Cerambycidae) is one of the most damaging pests of Japanese cedar (Kobayashi 1985). In central Japan, the life cycle of S. japonicus is usually completed in 1 year (Kobayashi and Shibata 1985). Mature adults emerge in spring, mate on the surface of the trunk soon after emergence, and the females lay their eggs in bark crevices. Newly hatched larvae enter the bark and feed in the cambial region, primarily on the inner bark (Kobayashi 1985). The larvae usually molt four times (Maeto 1985). Full-grown larvae enter the wood in late summer, pupate in cells in autumn, and overwinter as adults.

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Population fluctuations and outbreaks of S. japonicus in Central Japan are as follows (Ito 1999b): Semanotus japonicus established a population in the stand 5 years after planting. It continuously increased in numbers, reached a peak abundance 6 years later, and subsequently declined rapidly. This insect damaged ca. 50% of the initial tree population during the outbreak and ca. 35% of the infested trees were killed. The number of adults that emerged from each tree was correlated positively with tree diameter. Particular trees tended to consistently produce more adults during the outbreak than other trees. Larger, faster-growing trees were more vulnerable to mortality due to S. japonicus attack. The depletion of favourable host trees led to the collapse of the outbreak. This insect attacks living cedar trees with larvae mainly feeding in the inner bark (or phloem) of the trunk. There is a great variation in S. japonicus adult body size (Kobayashi and Shibata 1985). Enhanced nutritional conditions of the inner bark, i.e. nitrogen concentration and water content, could affect borer development (Shibata 1998). Primary borers are able to attack a healthy, living tree and complete their normal development, whereas secondary borers are incapable of attacking and completing normal development in healthy trees (Knight and Heikkenen 1980). Shibata (1995, 2000) hypothesized that Semanotus japonicus was placed in a transition category between primary and secondary borers, or in other words a ‘weak’ primary insect: S. japonicus may be trapped by ‘resin flow’ if they attack vigorous living trees or die due to ‘poor nutrition’ if they attack dead trees. Semanotus japonicus lives in a delicate balance with its host tree. Resin exuded by infested Japanese cedars is important as a mechanisms of host resistance to larval feeding by S. japonicus (Kobayashi 1985; Shibata 1987), although Japanese cedar normally lacks resin-producing structures. It is known that Japanese cedar forms traumatic axial resin ducts and produces resin in the inner bark in response to various kinds of injuries, including feeding damage by S. japonicus (Yamanaka 1984; Ito 1998). Only the 1- and /or 2-year-old growth layers of the inner bark were capable of forming new resin ducts in response to injury (Kanazashi et al. 1988; Ueki et al. 1989, Arihara and Suda 1996). This traumatic resin flow has been considered as the most important determinant of resistance to S. japonicus (Ito 1998, 1999a). Spatial extent of inducing traumatic resin ducts is different among individual trees and is an important determinant of tree resistance to this insect (Ito 1998). In some trees, resin duct formation was confined to the proximity of each larval gallery. However, in other trees, induction of resin ducts was extended throughout the whole trunk. Larval mortality was higher in trees that exhibited systemic induction of resin ducts than in other trees that showed a localized response. Time lags in inducing traumatic resin ducts and chemical and physical characteristics of resin are also possible factors related to the resistance. However, these factors have not been well studied. Under the leadership of the Forestry Agency Japan, a project to breed Japanese cedar that are resistant to S. japonicus started in 1985. Forest Tree Breeding Centres, Regional Forest Offices, and ca. 80% of Prefectures in Honshu and Shikoku Islands participated in the project. Four screening procedures have been conducted in the project (Ueki 1999). First, individuals that suffered no injury from S. japonicus

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were selected from heavily infested stands. From Honshu and Shikoku Islands, a total of 1413 individual trees were selected as candidates. Second, resistance of these trees were checked by pricking them with a pin. Formation of traumatic resin ducts and secretion of resin were the screening criteria. Third, a primary screening test was conducted in cages in which S. japonicus adults were released. Candidate tree clones (four trees per clone) were divided into five categories according to the average number of feeding signs on the sapwood in each clone. The clones in the lowest of the five classes passed the primary screening test. Then for each of the clones that passed the primary test, three fresh trees of each of these clones were subjected to a secondary screening test, in which 10 hatched larvae were inoculated on the outer bark. Only trees that were successfully inoculated were used in the secondary test; inoculation was considered successful when at least 4 of the 10 larvae showed feeding signs on the inner bark. If a tree was not successfully inoculated, another fresh tree of the same clone was inoculated. When no feeding signs were found on the sapwood of any of the three successfully inoculated trees of each clone, the clone was considered “resistant”. However, a few “resistant clones” could completely inhibit injury by this insect (Ueki 1999). Even on the same clone, the number of feeding signs of hatched larvae on the inner bark and on the sapwood varied greatly by both year and location in which the screening tests were conducted. The number of feeding signs was strongly influenced by environmental factors. Kato (2001) reported a low relationship between the ability of traumatic resin duct formation evaluated by a prick-with-a-pin method and the resistance to S. japonicus. This is partially because the ability of traumatic resin duct formation of the Japanese cedar varies greatly among individual trees (Kobayashi and Shibata 1985; Tajima 1986; Miyaura and Yamada 1991). In addition to traumatic resin-duct formation, the thickness of the inner bark was shown to be an important determinant of larval attack success (Arihara and Kawakami 1998). In trees in which traumatic resin-ducts are normally induced, insects could grow in the following way (Figure 3): First, larvae fed on the outermost layer of the inner bark, in which no traumatic resin ducts were formed and no resin was secreted. Thereafter they moved to the lower portion in which the conducting system had already been destroyed and formation of traumatic resin ducts was not so active. In trees with thin inner bark, larvae will be killed by resin because young larvae must feed on the innermost layer of the inner bark in which traumatic resin ducts will be formed. Resistance of Japanese cedar to S. japonicus is determined primarily by the formation of traumatic resin ducts but secondarily by the thickness of the inner bark. Its mechanism seems highly complicated and is likely to be a polygenetic trait (Ueki 1999).

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EPILOGUE In this paper, development of tree resistance to pests in Asia was reviewed. The information was mainly available from China, South Korea, and Japan in East Asia and amongst these three countries, most of the information was from Japan. Techniques of tree breeding have progressed greatly with the progress in molecular genetics. However, among all the tree breeding projects in Asia, there is still not one in which resistance mechanisms, substances related to it, and related genes are fully understood. For example, MAS using DNA markers is now available for breeding P. thunbergii that are resistant to the pine needle gall midge, although the mechanism of the resistance is still unclear. Breeding trees that are resistant to pests should be carried on by elucidating the resistance mechanisms, development of selection assisted by chemical substances, and development of a MAS method by elucidating related genes.

ACKNOWLEDGEMENTS I express my sincere thanks to Drs. Eui-Rae NOH (Former Director, KFRI, South Korea), MENG Yangqing and HAN Yifan (CAF, China), Kazutaka KATO and Eiji HAYASHI (FTBC, Japan), Takashi DAIDO and Yoshiaki NAGATA (Oji Tree Breeding Research Centre, Japan), Kazuyoshi FUTAI (Kyoto University), and Kenji FUKUDA (The University of Tokyo) for providing useful information. I also thank to Eiichi SHIBATA, K. FUTAI, Kensuke ITO, K. KATO, and E. HAYASHI for reviewing the earlier draft of this article. I am grateful to Prof. Dr. Michael R. WAGNER for his helpful comments. Yiqun LIN helped with the manuscript. I also thank her.

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CHAPTER 13 USING RESISTANCE IN TROPICAL FOREST PLANTATIONS

J. DOLAND NICHOLS1, MICHAEL R. WAGNER2, JOSEPH R. COBBINAH3

1. School of Environmental Science and Management, Southern Cross University, Lismore, NSW, Australia 2480 2. Northern Arizona University, Box 15018, Flagstaff, AZ, USA 3. Forestry Research Institute of Ghana, University Box 63, Kumasi, Ghana

1. PLANTATIONS IN THE TROPICS Technically speaking the tropics are centered around the equator, extending from 23 ½ ° N to 23 ½ ° S latitude. But nearly “tropical” conditions – particularly the lack of frost – may extend well to the north and south of these lines. Plantations, especially those in the tropics, can be highly productive, if species and provenances are properly chosen, yielding up to 40 cubic metres of wood per hectare per year or more, in the case of Eucalypts in Brazil. This compares with a growth rate of usable timber in natural forests that varies from Providing these figures are correct and assuming a conservative average production of , Sedjo and Botkin (1997) estimate that an area in plantations of only 0.15 billion hectares, or 4% of the global forested area, could produce most of the of industrial wood consumed annually in the world. Although there is high rainfall throughout the tropics, especially near the equator, species and provenances need to be carefully matched to sites to achieve consistently high growth rates. Also, since insect population increases are not limited by frosts in most of the tropics and because monocultural stands of young rapidly growing trees may be an ideal food source for herbivorous insects, care needs to be taken with respect to pests. This of course should include the use of tree stock that is partially or completely resistant to major 287

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insect pests, as well as having high growth potential, good form, and other desired characteristics. 1.1 EXTENT Estimating the exact number of hectares of plantations in the tropics is difficult, given that much of the data is reported on a per-country basis, rather than by ecological or climatic zone. Brazil for example includes some areas of subtropical plantations as well as those that are truly in the tropics. Also, within the tropics there are temperate-like conditions at higher elevations, where considerable tree planting has been taken place, as in Mexico, Central America, Colombia, Peru, Ecuador, Kenya. Also, “plantation” is not clearly defined, extending from enrichment planting in native forest through standard monocultural tree plantations to various types of agroforestry systems. Some surveys include rubber (Hevea) and coconut (Cocos) as well as standard timber or pulp producing species. Nevertheless, estimates of the total area in the tropics under plantations range from 30 million in 1990 (FAO, 1997) to as great as 42 million ha (Evans, 1992), while the latter source includes areas in warmer parts of the subtropics. The FAO (2001) estimated 51 million ha, when counting all of India as well as Brazil as “tropical”. In 1990 Eucalyptus spp. accounted for 23% of the total area planted in the tropics, followed by Pinus spp. (10.5%), Acacia spp. (7.7%) and Tectona grandis (5%) (FAO, 1997). Estimates of these proportions had shifted somewhat by the year 2001, with Eucalyptus at 26.2%, Pinus at 10.9%, Acacia at 14.9%, and Tectona grandis at 10.3% (FRA, 2001) (Table 1). In tropical Africa, about half of the plantation area is occupied by eucalypts and pines (mainly Pinus patula). In the moist parts of West Africa are Gmelina arborea, Terminalia superba and T. ivorensis, and mahoganies, especially Khaya species. In drier areas in Africa Acacia mearnsii is planted for tannin production, A. Senegal for gum arabic. Finally, the Asia/Pacific region has the most diversified plantation sector with eucalypts and pines on 20% of the total area, with the rest mainly occupied by Tectona grandis, Acacia spp., Dalbergia sisso, Paraserianthes falcataria, Casuarina spp., Gmelina arborea, and Swietenia spp. (FAO, 1997). Although large-scale plantations tend to be of exotic species, there are of course hundreds of native species in the tropics with potential to be used in plantations. Considerable information on these species is contained in older works on their silvicultural characteristics (Taylor, 1960), in summaries of newer research trials (Cameron and Jermyn, 1991; Haggar et al., 1998) and informal reviews of regionally-based knowledge (Nichols and Gonzalez, 1992).

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2. INSECT OUTBREAKS IN TROPICAL PLANTATIONS Insect outbreaks may be more or less common in tropical plantations, depending on a complex of factors, which are discussed near the end of this chapter. Speight (1997) listed four major causes for insect pest outbreaks in the tropics: 1) Natural disasters – fire, cyclones, drought, and unexpected frost. These events can create stressed trees and-or produce food or breeding sites. 2) Tree stress and susceptibility through management. This includes the allimportant but often neglected art and science of matching species and provenances with sites. It also involves good nursery management and the production of healthy seedlings, the choice whether to plant monocultures or mixed-species plantings, silvicultural manipulation, particularly thinning to relieve drought and other stresses, and post-harvest treatments, especially removal or burning of slash. 3) Pest invasions. These can be from outside the country, mainly accidental imports, and from inside the local area or region. 4) Misuse of control systems. This can mean manipulating a system so that natural enemies are lost or that tree stress is encouraged by use of phytotoxic chemicals. 2.1 TYPES OF RESISTANCE One way of categorising resistance is to divide resistance to insect attack into three major types (Gullan and Cranston, 2000; Watt et al., 2001): 1) Antixenosis, or non-preference, in which a plant is not preferred for use (feeding, oviposition). 2) Antibiosis, in which insects perform more poorly than on non-resistant plants, taking longer to complete their life cycles, having greater mortality, or having less reproductive success. 3) Tolerance, in which a plant can be attacked but maintains health and growth, recovering from insect attacks. The differing forms of resistance are quite complex, often difficult to distinguish from environmental effects, and may or may not be directly inherited. In any case, the nature of the plant, whether chemical, morphological or physiological, causes a response in the insect. Physical characteristics such as hairiness or leaf toughness may deter insect feeding and-or slow it down; plant chemicals may cause insects to develop more slowly or even die; and some resistant plants be “tolerant” in that they

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grow especially quickly through the stage at which they are susceptible (Watt et al., 2001). Among the many physiological forms resistance takes are: differences in morphological structures and tissue strength, in the exudation pressure and quantity and quality of gums and resins, differences in nutrient levels, hormonally active compounds in the plant, chemical behavior modifiers, protective substances, sensitivity to injury, phenology of flowering, leaf flushing and other processes (Barbosa and Wagner, 1989; Watt et al., 2001). To what extent resistance is acceptable depends largely on the type of damage done. Considerable foliar feeding can take place, even to the extent of several events of nearly total defoliation, without destroying the long-term potential of a sapling to become a well-formed tree. But only a few attacks by a shoot- or stemboring insect can ruin the form of a tree, rendering it economically worthless. 2.2 TROPICAL TREES AND RESISTANCE It can be argued that some temperate forest species, such as Douglas-fir, Pseudotsuga menziesii in the Pacific Northwest of the USA, or various pine species in the Southeast, tend to form nearly pure stands naturally and have evolved mechanisms for co-existing with herbivorous insects. But in the tropics, particularly in humid lowland rainforests, there is a high diversity of tree species and one of the most often invoked theories to explain this phenomenon is the Janzen (1971)Connell (1970) hypothesis, also called the “Escape Hypothesis”. They argue that predators on seeds and species-specific herbivores on seedlings are quite dense near mother trees and tend to eliminate all progeny in the immediate vicinity of those trees, with only the occasional seedling “escaping” by being at some distance away from its parent. Thus creating pure stands of single species would not mimic the diversity of tropical rainforests and those plantations would not be “resistant” to pests and would be inviting major outbreaks. 2.3 DETERMINING THE PRESENCE OF RESISTANCE Determining whether a given provenance or clone is truly resistant to a specific insect pest is not as straightforward as it might appear at first glance. One technique is simply to look through plantations under attack for apparently resistant individuals. Whether these have escaped merely through chance or perhaps flushed later or earlier than other trees within the plantation are possibilities, as well as their being genetically resistant. The other technique is of course to plant replicated trials of a group of species and-or provenances or even known genotypes and assess their performance in relation to a given pest. Then a decision would have to be made which considers resistance to one pest in the context of the relative growth rates of the tree species or provenance, its wood quality, site adaptations, susceptibility to other insect pests and diseases, and the maintenance of genetic diversity. So simply having some resistance to a given insect of course cannot be the only criterion for selection.

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In several cases, there is a complex of tree species within a genus or genera as well as a complex of insect species within a genus. Thus the search for resistance may span a group of species. Often the most commonly planted and most available species is the one which is most susceptible to pest damage. In the genus Leucaena, in addition to intraspecies evaluations of resistance by provenance or genotype, comparative evaluations have been made of the growth and resistance to the Leucaena psyllid Heteropyslla cubana Crawford (Homoptera: Psyllidae) of species other than the commonly planted L. leucocephala (Austin et al., 1995). The same sort of pattern is seen with Cupressus lusitanica and other species within the Cupressaceae, with respect to their resistance to the cypress aphid Cinara cupressi (Obiri, 1994). 2.4 MAJOR TROPICAL FORESTRY PLANTATION SPECIES 2.41 The Meliaceae Among the most valued of tropical timbers are those coming from several genera in the Meliaceae, particularly members of the sub-family Swieteniodeae. These include Swietenia macrophylla Jacq. (American mahogany) and Cedrela odorata L. (Spanish cedar) from the American tropics, Toona ciliata M. Roem from Australia and Papua New Guinea, and various Khaya spp. from Africa. The major pest of this sub-family is the mahogany shoot borer Hypsipyla grandella Zeller (Lepidoptera: Pyralidae) from the neotropics and Hypsipyla robusta Moore from Africa and the Asia/Pacific region. The larvae from these moth species bore into the tips of young trees and cause bifurcations, rendering the tree economically worthless (Newton et al., 1993; Mayhew and Newton, 1998; Watt et al., 2001). Recent taxonomic assessment suggests there are probably eleven species of Hypsipyla world wide, but H. grandella and H. robusta are still likely the most important species (Horak 2001). There have been some indications that exotic species of the Swieteniodeae are less susceptible to the local species of Hypsipyla, that is African and Asian Meliaceae. should do better in the Americas and American tree species should suffer less shoot boring when planted in the Asia-Pacific region or in Africa. Eventually one would expect a breakdown of the defenses to whichever species of the shootborer is present (Zobel et al., 1987), Swietenia macrophylla from the Americas was perhaps at first resistant to H. robusta when planted in the Asia/Pacific region but reports from countries in the area indicate this is no longer true (Floyd and Hauxwell, 2001). Similarly, although Cedrela odorata has been grown successfully in Ghana (Atuahene, 2001), it is attacked by H. robusta in Australia (Cameron and Jermyn, 1991). Khaya spp. from Africa have been grown without attack in Latin America and Toona ciliata from Asia/Pacific has demonstrated some resistance to the American H. grandella (Watt et al., 2001). For example, Rodriguez (1980) found in Cuba that Khaya myasica, K. senegalensis and K. ivorensis showed high levels of resistance to H. grandella. In areas that are naturally Hypsipyla-free there are still productive S. macrophylla plantations, including in Samoa and Fiji. Unfortunately, simply recommending that exotic Meliaceae be planted, in pure

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stands and with no silvicultural manipulations, “is not the answer to the shoot borer problem” (Watt et al., 2001). The mechanisms for resistance in the Meliaceae are complex, involving growth rates, the phenology of leaf production, and nutrient and secondary compounds in foliage. Newton et al. (1998, 1999) reported on progeny/provenance trials of Cedrela odorata and provenance testing of Swietenia macrophylla in Costa Rica in which intensive assessments were made over 84 months. Height growth by provenance was significantly different in both species. C. odorata from a wet zone provenance remained foliated but more than 35% of the leaves of dry zone trees abscised during the dry season. The mean number of attacks during the peak of attack (during the second year of growth) varied significantly by provenance for both tree species. A provenance from San Carlos, Costa Rica was subjected to fewer attacks during the first year and had a significantly higher mean height to first point of damage. In this provenance foliar nitrogen concentration was significantly lower and tannin and proanthocyanidin contents significantly higher than in the other provenances. Thus both vigorous apical growth (tolerance) and foliar chemical content (possible antibiosis) were found to be components of partial resistance to the shoot borer . A poll rating research priorities by persons attending a conference of Hypsipyla placed research on resistance trees above all other priorities (Floyd, 2001). The role of resistant in developing integrated pest management in plantation programs for the Meliaceae is discussed at the end of this chapter. 2.4.2 Tectona grandis Teak is one of the world’s most prized woods, having been long appreciated for its resistance to decay and for its attractive timber. Teak is native to India, Myanmar, Thailand and Laos and marks the one exception to the general rule that successful tropical plantations are of exotic species, with considerable areas of teak being grown in the countries where it is native. Approximately 400 to 600 years ago teak was introduced to Java, Indonesia, where it now naturalised and there are some 1.5 million ha of plantation. The total planted around the world is somewhere between 2.2 and 5.7 ha. (FAO, 2001; Pandey and Brown, 2001). Perhaps the most serious pest of teak is the teak defoliator Hyblaea puera (Lepidoptera: Hyblaeeaidae). The larvae of this moth can cause significant defoliation in teak plantations. As Speight and Wylie (2001) point out, a study by Nair et al. (1989) indicated initially that two clones of 25 appeared to have much lower susceptibility to this herbivore. But subsequent studies showed that those two clones were in fact no more resistant to defoliation than the other clones tested and merely out of some unexplained phenomenon were not attacked early in the study. In searching the Indian state of Kerala for resistant clones in plantations, natural forests and seed orchards, they encountered unattacked trees, but concluded that this was due to “phenological resistance”, that is some trees did not make tender foliage available at the right time in the insect’s life cycle. But this characteristic was not consistent over several years and therefore could not be used in breeding programs.

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Avinash et al. (1998) further evaluated the variation in resistance to H. puera as well as to the teak leaf skeletonizer Eutectona machaeralis (Lepidoptera: Pyralidae). They found that over a 4-year period, of some 167 clones from 10 Indian states, two, ORANR-3 and APT-14, could be identified as the most resistant and most susceptible. They also categorized the remaining clones into eight different levels, from highly resistant to most susceptible. Foliar phosphorus, calcium and magnesium were significantly higher in the most resistant clone and lower in the most susceptible, while chlorophyll a and b were at a minimum in the most resistant, and a maximum in the most susceptible. In further studies on yet another teak defoliator, the leaf skeletoniser Paliga machoeralis (Lepidoptera: Pyralidae), Avinash et al. (2000) analyzed leaf protein and polyphenol contents for selected resistant and susceptible teak clones. The protein and polyphenol contents of clonal leaves were directly and inversely proportional to the amount of leaf damage, so that a low protein:polyphenol ratio was associated with higher resistance and vice-versa. Roychoudhruy and Joshi (2000) also found that the most resistant and susceptible clones in the studies by Avinash had the same response to a nursery pest, Spodoptera litura (Lepidoptera: Noctuidae). 2.4.3 Pinus species The pines illustrate the complexity of matching species with site as well as finding the species most resistant to the insects which are likely to become pests in a given area. Among the pines planted in the tropics are P. caribaea, P. patula, both native to the Americas, and P. merkusii, native to Sumatra in Indonesia. One of the problems with pines as well as other species is that the best growing, most wellknown species or subspecies are: 1) the most susceptible to certain insect pests and 2) their seed is the most available. For example, Cremiere and Ehrhart (1990) reported on 30 years of experience with pines in New Caledonia and concluded that Pinus caribaea subsp. hondurensis had the best performance overall, in terms of tree growth, mortality, shape and resistance to both cyclones and fire. But this pine, one of the most widely planted in the tropics, is, as Speight and Wylie (2001) point out, in some areas the most susceptible to local insects. In the Philippines, Speight and Speechly (1982) recorded heavy attacks by pine shoot moths, Rhyacionia and Dioryctria spp. (Lepidoptera: Tortricidae and Pyralidae) on the P. hondurensis subspecies. Another variety, P. caribaea var. bahamensis is almost completely resistant (Baylis and Barnes, 1989). But seed of the hondurensis subspecies was what was available, well known, and therefore planted. In other areas, P. caribaea might be the best choice not only for its desirable growth properties but also for its resistance to Dioryctria larvae; in Indonesia the indigenous species P. merkusii was more susceptible to Dioryctria damage than either P. caribaea or P. oocarpa, both from the Americas (Intari and Ruswandy, 1986).

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2.4.4 Eucalyptus species There are more than 500 species of Eucalyptus native to Australia; they occur naturally from near-rainforest conditions to low semi-arid woodlands (Eldridge et al., 1994). Several of these have become of great importance as exotics in plantations, with more than 20 species being planted commercially in about 50 countries (Ohmart and Edwards, 1991). Although some 96 indigenous herbivores have adapted to feeding on eucalypts in different parts of the world, generally they appear to have caused little harm, while insects native to Australia which have been accidentally introduced have been responsible for much more damage (Ohmart and Edwards, 1991). Termites have caused major mortality of eucalypt seedlings in tropical and subtropical regions so that, without control measures, plantations may not be established. In Brazil and other parts of the American tropics leaf-cutting ants, particularly those in the genus Atta, can also cause defoliation and tree mortality. There have been at least 21 species of Australian insects recorded overseas on eucalypts. The most widespread of these is the stem-borer Phoracantha semipunctata (Coleoptera: Cerambycidae), having the biggest impact in countries where droughts are frequent, and providing a good example of the need to plant drought-tolerant species in drought-susceptible areas (Speight and Wylie, 2001). A weevil, Goniptera scutellatus (Coleoptera: Curculionidae), is the other major pest, which caused major defoliation of eucalypts, particularly in South Africa, but has been brought under control by the use of an egg parasite. Strepsicrates rothia, Meyrick (Lepidoptera: Tortricidae) occurs in humid tropical Africa. In Ghana, it has been recorded on E. tereticornis and other eucalypt species (Cobbinah, 1973). E. tereticornis is the most preferred species. The larvae roll single leaves of eucalyptus, forming a shelter in which it feeds and rests. Damage to eucalyptus seedlings is high at the beginning of the dry season and seedling mortality may exceed 50%. Among the most important planted eucalypts is E. camaldulensis (river red gum), a highly variable species, and the most widely distributed in its natural range, from below 13° S to above 38° S latitude. E. camaldulensis is perhaps the most widely planted tree species in arid and semi-arid areas of the world (Eldridge et al., 1994). In the 1980s some two tons of seed was exported annually from the northern (tropical) Australian provenances (one ton yielding approximately 600 million germinants). Mitchell and Boland (1989) tested a large number of tree species in Zimbabwe, looking at growth rates and at resistance to termites. E. camaldulensis had the second-highest growth rate but two-thirds of its seedlings were killed by termites during the establishment phase. On the other hand, Oliveira et al. (1984) studied the resistance of 11 eucalypt species to the defoliator Thyrinteina arnobia (Lepidoptera: Geometridae) in Brazil, and found E. camaldulensis to be the most resistant. E. tereticornis (forest red gum) is closely related to E. camaldulensis. Its natural range was extensive, covering some 30° of latitude, from southern Papua New Guinea through the summer rainfall region in Queensland down to the cool, wet winter rainfall climate in Victoria. E. tereticornis tends to be more of a coastal

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species than E. camaldulensis although there is a considerable zone of overlap where trees with intermediate characteristics are found, in northeast Queensland. Eucalyptus grandis forests are native to northern New South Wales and southeast Queensland, with another population found in northern Queensland, in both cases within 100 km of the sea. Generally E. grandis is one of the fastest growing trees on good sites in subtropical and warm temperate sites while pure E. grandis is not considered suitable for lowland regions in the humid tropics (Evans, 1992). E. grandis may occupy the greatest area of plantation for industrial wood production of any eucalypt, with well over one million hectares in Brazil and large areas in South Africa. In what may well be a sign for the future, Harcourt et al. (2000) reported on the development of insect- and herbicide-resistant transgenic eucalypts. They used an Agrobacterium tumefaciens-mediated transformation of seedlings to produce E. camaldulensis containing the insecticidal cry3A gene and the bar gene. The former gene gave resistance to first instars of chrysomelid beetles and the latter gene provided tolerance to the broad-spectrum herbicide glufosinate ammonium. The authors stressed the importance of assessing and minimizing any adverse impacts of wide scale planting of transgenic eucalyptus. There are only two eucalypts species which do not occur naturally in Australia, and both are planted extensively throughout the tropics. One of these is E. deglupta, native to Mindanao in the Philippines, Sulawesi and Irian Jaya in Indonesia, parts of Papua New Guinea, and on most of New Britain (Eldridge, 1994). E. deglupta is well known for its impressive growth rates on good sites ( over 15 years). But it is demanding in terms of site, can burn easily, does not coppice as easily as many eucalypt species do, and is susceptible to some diseases as well as insect pests, including termites. The countries with the largest plantations are the Philippines, Indonesia and Brazil, with perhaps 100,000 hectares having been planted worldwide (Eldridge, 1994). The varicose borer Agrilus sexsignatus has been a cause of major mortality in E. deglupta plantations of the Paper Industries Corporation of the Philippines (PICOP) since 1975. Braza (1987a) pointed out that previous studies had suggested that only trees under stress were attacked by the borer. He implanted borer larvae into healthy plantation trees and found that larval development was prolonged and larval survival quite low on an indigenous provenance of E. deglupta, in contrast to the heavilyattacked Papua New Guinea provenance. Thus a local native tree species may in some cases have an advantage over an exotic species or provenance which has not evolved any resistance mechanisms to cope with a given pest. The other non-Australian eucalypt is E. urophylla S.T. Blake, native to Timor and several nearby islands in Indonesia between 7° 30 S and 10° S. In the case of a white grub Leucopholis irrorata (Coleoptera: Scarabidae) in the Philippines, E. deglupta, E. urophylla, Acacia mangium and Pinus caribaea, had their roots fed upon heavily. Braza (1987b) recorded mortality rates of 50-80% after two weeks exposure. This is an example of a generalist rather than monophagous pest which, like leaf-cutting ants, is difficult to control. For a discussion of E. grandis x E.

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urophylla crosses and their resistance to one pest species, see the section below on hybrids. 2.4.5 Acacia species Acacia mangium is native to the the Moluccas, Irian Jaya and northern Queensland in Australia. It the 1960s it was introduced to Sabah, Malaysia where it is a major component of a 200,000 ha reforestation program. A. mangium is also of great importance in Indonesia, where it has been highly productive in reforestation programs on vast areas of degraded Imperata cylindrica grassland, with there now being at least 500,000 ha planted, mostly in Sumatra and Kalimantan (Nair and Sumardi, 2000). Thus, although A. mangium is native to Indonesia it is only so in a very small part of the country and can be considered an exotic throughout most of that country. The sap-sucking mosquito bug, Helopeltis spp. (Hempitera: Miridae) is a common pest on several horticultural crops as well as on Acacia mangium. Feeding by Helopeltis causes necrotic spots and often dieback of young shoots (Wylie et al. 1998) and represents the most serious insect threat to A. mangium plantations in Indonesia (Nair and Sumardi, 2000). Other pests include the subterranean termite, Coptotermes curvignathus (Isoptera: Rhinotermitidae) which can kill 10-50% of saplings by eating into the taproot and stem (Wylie et al., 1998) and several pinhole borers in the genus Xylosandrus (Coleoptera: Scolytidae). Not a great deal of work on resistance to insects in tropical acacias appears to have been done (Wylie et al., 1998; Nair and Sumardi, 2000). In a comparison of early performance of Queensland and Papua New Guinea (PNG) provenances of A. crassicarpa, Otsamo et al. (1999) found that there were no significant differences in occurrence of pests and diseases among the PNG provenances but that the PNG provenances had a higher proportion of trees affect by borers (Xyleborus spp., Coleoptera: Scolytidae) than the Queensland provenances. In another case Faizuddin and Dalmacio (1992) found great variability to pests and diseases in different provenances of A. mangium in platations in the Philippines. 2.4.6 Cupressus lusitanica Cupressus lusitanica, native to highland areas of Mexico, Guatemala and El Salvador, has been widely planted in mountainous areas in the tropics, particularly in East Africa. Its major pest is the cypress aphid Cinara cupressi (Murphy 1998). To assess other related conifers Obiri (1994) reviewed the growth rates and tolerance of the aphid on 24 species within the Cupressaceae in Kenya. Thuja spp. and Chamaecyparis leylandii were the most tolerant. Several of the cypresses, Cupressus torulosa, C. funebris and C. arizonica were very resistant while the commonly planted C. lusitanica was found to be susceptible. Kamunya et al. (1997, 1999) studied genetic control of resistance to Cinara cupressi. They concluded that there was a strong additive genetic element in resistant trees of C. lusitanica, and that genetic correlations between aphid damage and growth characteristics were not significant, so that selection for resistance would be unlikely to have a negative effect on these economic traits.

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2.4.7 Milicia species Milicia excelsa and M. regia are important timber species across Africa from Kenya to Senegal. Their situation is similar to that of many of the Meliaceae: in natural forests Milicia occurs in low densities and when established in plantations it is severely attacked by an insect, prohibiting production to date from other than natural forest. Again, as in the case of the mahoganies, developing tree resistance to the pest is part of a strategy to grow it successfully (Wagner et al., unpublished data). Perhaps no tree in tropical Africa has been studied more intensively for resistance than Iroko (Milicia spp.). The pest, Phytolyma lata, a gall forming psyllid, attacks seedlings and saplings of Milicia forming globular galls. When galls burst to release adults, the surface fluid is colonised by saprophytic fungi, which cause dieback. In nurseries and young plantations, large numbers of galls on leaves and petioles lead to loss of leaves and often times seedling mortality. Prospects for reducing the impact of P. lata increased with the observation of partial resistance within natural populations (Cobbinah, 1990). Progeny evaluation by Cobbinah and Wagner (1995) indicated highly significant variation among 21 half-sib families in growth and resistance to galling. Further, Ofori et al. (2001) and Appiah et al. (In press) recorded significant differences among populations and provenances from Ghana, Cote d’lvoire and Sierra Leone with regard to growth performance and resistance to P. lata attack (Figure 1). Family and clonal heritability values of 0.94 and 0.3 respectively were observed. Selective removal of less desirable genotypes resulted in genetic gains of 12 cm in height growth in three months and 22.8 cm in two years for progeny and clones respectively (Ofori et al. 2001). RAPD survey of natural populations of Milicia indicated a substantial degree of genetic variation which is ecologically structured (Ofori et al. unpublished data). Earlier anatomical (Djabletey, 1994) and chemical (Gbowonyo et al., unpublished data) studies indicated that resistant genotypes have two fold more tannin containing cells and more total phenols and phenolic oxidase activity than susceptible genotypes. However, because of the likelihood that resistance could break down, an Integrated Pest Management strategy has been developed for P. Lata (Cobbinah, 1990; Wagner et al., 1991).

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2.4.8 Leucaena species Leucaena species, particularly L. leucocephala (Lamb.) de Wit, native to Mexico and Central America, have been widely planted as agroforestry species around the world in the tropics. Leucaena is a fast-growing nitrogen-fixing tree, useful in alleycropping, for soil conservation and enrichment, and as fuelwood and fodder. One of the major problems Leucaena has had is the leucaena psyllid, Heteropsylla cubana Crawford (Homoptera: Psyllidae). The psyllid has spread to the Asian/Pacific region, causing serious devastation, even at moderate damage ratings, with yield loss in dry weight often being >50% (Mullen et al., 1998). H. cubana was the subject of a workshop (Napompeth and MacDicken, 1990) and continues to be widely studied. Considerable variation has been found in resistance to the leucaena psyllid both within and among species (Napompeth and MacDicken, 1990; Austin et al., 1995; Mullen et al., 1998). Generally L. leucocephala – like P. caribaea the most commonly planted and available tropical species in the genus – has proven to be the most susceptible. Other species, particularly L. diversifolia (Austin et al., 1995; Hosalli and Kulkarni, 2000) and L. collinsii (Lapis and Borden, 1993), have been much more resistant, as well as L leucocephala x L. diversifolia hybrids (Elder et al., 1998) and some cultivars of L. leucocephala (Austin et al., 1995). Ultimately, resistance to the psyllid is only one of several desired characteristics selected for in

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breeding programs; strategies in Hawaii and Brazil are based on using tetraploidlevel crosses of L. leucocephala, L. pallida and L. diversifolia to achieve several objectives, including psyllid resistance, increased biomass yield, cold tolerance, andor acid-soil tolerance (Austin et al., 1997, 1998). In this case wood production is not as important as dry weight production of forage. But the quality of that forage must also be considered. As Speight and Wylie (2001) point out, the secondary chemicals (possibly tannins) which make species or genotypes of leucaena psyllidresistant may also make it less palatable to livestock, so that resistance has to be balanced with other characteristics. 2.5 HYBRIDS AND RESISTANCE In many cases insects are more diverse and abundant on hybrid trees than on pure species, whether those trees occur in natural forests or plantations (Floate et al. 1993; Fritz, 1999; Whitham et al., 1999). To judge the effect of plant genetics on arthropod richness and composition, Dungey et al., (2000) examined arthropod communities on both artificial and wild populations of Eucalyptus amygdalina, E. risdonii and and hybrids. Different communities were supported on pure species and hybrid populations. In both artificial and wild populations the hybrids supported higher arthropod richness, with hybrids being a center of biodiversity by accumulating both common and specialist taxa of both parental species. In a review of 152 case studies of taxa associated with diverse hybridizing systems, Whitham et al. (1999) found that in 28% of cases, hybrids were more susceptible than their parent species. Thus planting pure stands of hybrids in the tropics would appear to be risky business, given that tropical trees naturally protect themselves by being rare and that hybrids often are more susceptible to pest and disease damage. The parent species in hybrids can contribute resistance or susceptibility to herbivores. Shepherd et al. (2000) examined variation and resistance to Christmas beetles, Anoplognathus porosus (Leach) (Coleoptera: Scarabaeidae) in Eucalyptus grandis and E. urophylla. E. grandis is native to the Christmas beetle home range, whereas E. urophylla is not. Backcrosses of E. grandis x E. urophylla to E. urophylla had higher amounts of leaf area consumed than other second generation controlled crosses (Figure 2). E. urophylla is a tropical eucalypt, not native to Australia, does not encounter A. porosus in its native habitat, and therefore may be the source of susceptibility to the beetle. Clones of E. grandis from open, drier forests, as opposed to tall moist closed forests, may represent a source of resistant individuals. Thus a native species which has co-evolved with an insect pest may transfer some resistant characteristics in hybrids.

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The implications for plantation forestry - particularly in the tropics – where tree species may not have evolved anti-pest mechanisms - is that care needs to be taken in committing to plant large areas with a small genetic base of hybrids, which may have desirable growth characteristics, yet be highly susceptible to potential insect pests. 2.6 DEPLOYMENT OF RESISTANT TREE STRAINS In a sense the most common form of resistance that is actually deployed is using an exotic tree. For the most part, large successful plantations of trees in the tropics are of species planted outside their native ranges (Table 1). Traditionally the focus of tree breeding for plantations has been on survival, growth, form (straightness being an especially heritable characteristic) and wood quality, and only secondarily on resistance to pests and diseases (Zobel et al., 1987). Aracruz Celulose in Brazil, represents one of the largest plantation efforts in the tropics, planting eucalypts for pulp production. Laranjeiro (1994) discussed the role of resistant stock in the company’s integrated pest management strategy. One technique used is to maintain 1 ha of native vegetation for each 2.4 ha of eucalypt planting, thus enhancing the presence of natural enemies of insects which may reach pest status. Also, systematic monitoring of insect levels is done, and occasionally

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various chemical sprays are applied, as is Bacillus thuringiensis. One of the most serious problems comes from leaf-cutting ants, in this case Atta sexdens rubropilosa. In eucalypt trials some 90% of plants were totally defoliated. The ants showed preferences that were categorized as high, medium and low. Laranjeiro advises that careful analysis of results be done, considering that preferences varied between species and provenances. Choosing clones solely on the basis of low leaf-cutting ant preference was not completely strategically suitable for integrated pest management of all pest species, or for maximum forest productivity and quality– it being judged not commercially viable to eliminate a clone with good productivity and quality only because it is preferred by ants. 2.7 RESISTANCE AND EXOTIC VERSUS NATIVE PLANTATION TREES Considerable confusion abounds on the topic of native vs. exotic tree species, natural forests vs. plantations, and monocultures vs. mixed-species plantations (Zobel, 1987; Gadgil and Bain, 1999). Although it would seem intuitive that mixed stands should be more resistant to insects and diseases, the vast majority of plantations in the tropics as well as in the temperate zone are monospecific, given that it is considered impractical to plant and harvest several different species. Since large areas in temperature North America are naturally occupied by single (or nearly single) species stands, particularly by Pinus spp. in the West and Southeast and Pseudotsuga menziesii in the Northwest, often resulting from large-scale fires, it has seemed reasonable to use pure plantations of those species, which may well have evolved their own mechanisms for co-existing with indigenous insect populations. But in the tropics, where highly diverse forests are the norm, it would appear to be a risky strategy to plant monocultures. This is where the issue of exotic vs. native species comes in: most tropical plantations to date, have been of exotic species, either exotic within a region, or more commonly exotic by originating on other continents. Rubber (Hevea braziliensis) coffee (Coffea arabica and C. robusta) and cacao (Theobroma cacao) are all examples of tropical plants which have been grown successfully away from their continents of origin. Similarly in plantation forestry, eucalypts from Australia and far southeast Asia, have been successful in India, China, the Americas, especially Brazil, and in South Africa. Likewise, tropical pines from Central America have had great success pantropically. The one great exception would be teak, Tectona grandis, which is grown in its native range in India, Myanmar, and Thailand as well as around the world. Teak may be somewhat different in that it is not native to equatorial regions with a year-round wet season but from areas with significant dry seasons. Also, the extractives which make it such a valuable timber may provide some resistance to insect pests. As Nair and Sumardi (2000) argue, it is difficult to make a generalization about whether exotic or native species are more pest-susceptible. In the case of Indonesia, most planted species are exotic and both exotic and native species have serious pest problems, with examples being the indigenous Pinus merkusii and the exotic Swietenia macrophylla. They point out that an indigenous species is unlikely to be destroyed completely, as it would have co-evolved with a given pest. But an exotic

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would be, at least for a while, free from pests native to its home range, although such pests, once introduced can have catastrophic impacts. Examples are the leucaena psyllid, conifer aphids, eucalypt trunk borers and the weevils. The exotic tree species may also be susceptible to local pests and diseases to which it has not adapted. The issue of native vs. exotic species is often confused with the differences between natural mixed stands and monospecific plantations. A large expanse of a native species of a limited genetic base, fast-growing, and producing nutritious, tender foliage, would seem to invite outbreaks of native pests, which are normally held in control by the diversity of tree species and age classes and a complex of natural enemies found in native forest. Thus developing a new set of influences artificially, using proper site-species matching, an understanding of pests’ life cycles, biocontrol agents, judicious spraying of pesticides in certain cases, silvicultural manipulations and genetically-based resistance would all be involved in developing successful tropical plantation regimes. 2.8 USE OF RESISTANT TREES AS PART OF AN INTEGRATED PEST MANAGEMENT STRATEGY Rather than taking the crude and expensive approach of simply spraying any pest species with toxic insecticides, integrated pest management aims to develop a sophisticated understanding of a given pest’s life cycle, and then to recommend appropriate, minimally invasive if possible, methods of management. These may include silvicultural techniques, such as regulation of stand density, pruning, etc., spraying at key times in the pest’s life cycle, the use of biocontrol organisms and the use of completely or partially resistant tree stock (Elliott et al., 1998). The role of resistant trees in an integrated pest management program can be considered in two major groups of species: Milicia species in Africa and the mahoganies (Meliaceae) pan-tropically. Wagner et al. (2000) outlined the components of a research program designed to develop production of Milicia in Africa. As discussed above, provenances resistant to the gall-forming psyllid Phytolyma lata have been identified and cuttings from them can be utilized in planting programs. But resistance is not total; in fact levels of dieback among more resistant stock are still not acceptable for commercial plantation forestry. So in addition to recommending the use of partially resistant trees, it could also be recommended that silvicultural techniques such as planting Milicia in low densities in a matrix of other plantation species or in native forest (enrichment planting) may enable some individuals to escape serious dieback. Further, exploration for biocontrol agents may yield some predators or parasitoids that can lower populations of P. lata (Bosu et al., 2001). In the case of the Meliaceae, Newton et al. (1993) suggested using resistant tree stock in combination with silvicultural methods, namely establishing mixed-species plantations or enrichment plantings in natural forest, although the exact requirements in terms of site-species matching, shade, densities, and so on are not known. They also advocated combining these methods with chemical and

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biological controls, while admitting that losses to Hysipyla would still take place. In a later assessment, Speight and Cory (2001) state that mahogany can still not be successfully grown, since Hysipyla is a pest which has high impact, making timber production uneconomic, at low insect densities. They propose that the development of an integrated pest management program for Hypsipyla spp. should involve several levels. The first of these can be called preventative, including careful site choice so that low tree vigor is avoided, selection of resistant species or genotypes, understanding the presence of pest in the region and nearby forests, designing silvicultural systems, and so on. The second stage involves on-going monitoring, particularly during vulnerable growth periods and devising a definition of economic threshold that would indicate the need for treatments. The third level covers control strategies which would have to be applied if prevention fails or modelling predicts a serious risk of outbreak. 3. SUMMARY Tropical forest plantations are a major source of wood fiber throughout the world. These plantations are subject to depredation by pest insects much like other forests of the world. The use of exotic species is a common form of managing forest pests, but this approach is not without limitations in general and is certainly not a sufficient control strategy to limit all pests. Substantial work has been done to understand mechanism of resistance in tropical tree species such as mahogany, teak, pine, eucalyptus, Leucaena, Acacia, and Cupressus. A pest-resistant transgenic Eucalyptus has been developed but is not operationally deployed. The substantial diversity of tropical trees represents both an opportunity to search for resistance to pests and a challenge to manage the huge array of current and potential forest insect pests. REFERENCES Appiah, M.K. Cobbinah, J.R. and Luukkannen O. (In press). Early growth performance of Iroko (Milicia excelsa) provenances grown under different environmental conditions in Ghana. Ghana Journal of Forestry (In press). Atuahene, S. K. N. 2001. The forest resources of Ghana and research on Hypsipyla robusta (Moore) (Lepidoptera:Pyralidae) control in mahogany plantations in Ghana. in Hypsipyla Shoot Borers in Meliaceae. R. B. Floyd and C. Hauxwell, (eds.). Symposium Proceedings, 20-23 August 1996, Kandy, Sri Lanka. Australian Centre for International Agricultural Research Proceedings No. 97, Canberra, Australia. 189 pp. Austin, M. T., Early, R. J., Brewbaker, J. L., and WeiGuo, S. 1997. Yield, psyllid resistance, and phenolic concentration of Leucaena in two environments in Hawaii. Agronomy Journal 89:507-515. Austin, M. T., Sorensson, C. T., Brewbaker, J. L., Sun, W., and Shelton, H. M. 1995. Forage dry matter yields and psyllid resistance of thirty-one leucaena selections in Hawaii. Agroforestry Systems 31: 211-222. Austin, M. T., Sun, W., Brewbaker, J. L., and Schifino-Wittmann, M. T. 1998. Developing leucaena hybrids for commercial use. ACIAR Proceedings Series 86: 82-85. Avinash Jain, Roychoudhury, N., Sharma, S., Bhargava, A., and Pant, N. C. 1998. Host plant resistance to insect-pests in teak (Tectona grandis L. f.) with reference to biochemical parameters. Indian Journal of Forestry 21:285-289.

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Avinash Jain., Roychoudhury, N., and Bhargava, A. 2000. Role of foliar protein and polyphenol and their relationship to clonal resistance in teak againist the leaf skeletoniser, Paliga machoeralis Walker (Lepidoptera:Pyralidae). Journal of Tropical Forest Science 12:221-226. Barbosa, P., and Wagner, M. R. 1989. Introduction to Forest and Shade Tree Insects. Academic Press, San Diego. 639 pp. Baylis, W. B. H., and Barnes, R. D. 1989. International provenance trials of Pinus caribaea var bahamensis. Forest Genetic Resources Information: 24-25. Bosu, P.P. Cobbinah, J.R. and Wagner, M.R. 2001 Feasibility of biological control of Pytolyma lata in Africa. International Tropical Timber Organization Odum Workshop Proceedings. Fumesua, Ghana. November 2000 (in press). Braza, R. D. 1987a. Growth and survival of varicose borer (Agrilus sexsignatus) larvae in Philippine provenance of bagras (Eucalyptus deglupta). Malaysian Forester 50: 235-238. Braza, R. D. 1987b. Resistance of seedlings of four plantation tree species to white grubs, Leucopholis irroata (Chevrolat) (Coleoptera:Scarabidae). Sylvatrop 12: 1-7. Cameron, D. M., and Jermyn, D., (eds.). 1991. Review of Plantation Performance of High Value Rainforest Species. Queensland Forest Service, CSIRO, Brisbane, Queensland, Australia. 60 pp. Cobbinah, J.R. 1990 Biology seasonal activity and control of Phytolyma lata (Homoptera:Psyllidae). In proceedings – IUFRO workshop. Pest and diseases of forest plantations. (Eds. Hutacharern C., Mac Dicken K.G., Ivory M.H. and Nair K.S.S.) pp. 180-185. FAO of United Nations, Bangkok, RAPA Publication. 1990/9. Cobbinah, J.R. 1973. Natural variation in susceptibility of four species of Eucalyptus to Strepsicrates rothia – Meyr (Lepidoptera:Tortricidae). Planning Branch Entomology Report 4, Ghana Forestry Department. Cobbinah, J. R., and Wagner, M. R. 1995. Phenotypic variation in Milicia excelsa to attack by Phytolyma lata (Psyllidae). Forest Ecology and Management 75:147-153. Connell, J. H. 1970. On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. Prc. Adv. Study Inst. on Dynamics of Numbers in Populations. P. J. der Boer and G. R. Gradwelleds, Center Ag. Publishing and Documentation, Wageningen: 298-312. Cremiere, L., and Ehrhart, Y. 1990. Thirty years of introduced pine species in New Caledonia. Bois et Forets des Tropiques 223: 3-23. Djabletey, G.D. 1994. Comparative leaf anatomy of resistant and susceptible leaves of Milicia species to Phytolyma lata. B.Sc. dissertation, KNUST 43pp. Dungey, H. S., Potts, B. M., Whitham, T. G., and Li, H. F. 2000. Plant genetics affects arthropod community richness and composition: evidence from a synthetic eucalypt hybrid population. Evolution 54:1938-1946. Elder, R. J., Middleton, C. H., and Bell, K. L. 1998. Heteropsylla cubana Crawford (Psyllidae) and Coccus longulus (Douglas) (Coccidae) infestations on Leucaena species and hybrids in coastal central Queensland. Australian Journal of Entomology 37:52-56. Eldridge, K., Davidson, J., Harwood, C., and van Wyk, G. 1994. Eucalypt Domestication and Breeding. Clarendon Press, Oxford. 288 pp. Elliott, H. J., Ohmart, C. P., and Wylie, F. R. 1998. Insect Pests of Australian Forests: Ecology and Management. Inkata Press, Melbourne, Australia. 214 pp. Evans, J. 1992. Plantation Forestry in the Tropics. Oxford University Press, Oxford. 403 pp. Faizuddin, M., and Dalmacio, R. V. 1992. Provenance variations of mangium (Acacia mangium Willd.) in survival and resistance to pests and diseases in the Philippines. Bangladesh Journal of Forest Science 21:46-53. FAO 1997. State of the World's Forests Food and Agricultural Organization of the United Nations, Rome. 202 pp.. FAO 2001. Forest Resources Assessment. Table 6:1(14) http://www.fao.org/forestry/fo/fra/index/jsp. Floate, K. D., Kearsley, M. J. C., and Whitham, T. G. 1993. Elevated herbivory in plant hybrid zones: Chrysomela confluens, Populus and phenological sinks. Ecology 74:2056-2065. Floyd, R. B. 2001. International workshop on Hypsipyla shoot borers in Meliaceae: General conclusions and research priorities. In: Hypsipyla Shoot Borers in Meliaceae. R. B. Floyd and C. Hauxwell, (eds.). Symposium Proceedings, 20-23 August 1996, Kandy, Sri Lanka. Australian Centre for International Agricultural Research Proceedings No. 97, Canberra, Australia. 189 pp.

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Keyword Index

abietic acid 123, 275 abiotic environment 3 abiotic factor 4, 247 abiotic induction 1 accidental introduction 67 activated defense 32 adaptation 5, 11, 65, 67, 108, 124, 176, 227, 258, 293 adapted insect 6, 7, 9, 12, 14, 90 additive inheritance 155, 159, 164 aggregation 35, 37, 47, 48, 50, 5660, 66, 67 aggressive agent 46, 139 aggressor 33-35, 39-41, 43, 44, 4651, 55, 56, 61, 64, 65, 67, 68, 243, 245, 247, 248 alkaloid 5, 11, 122, 125 allelochemical 81, 100 allocation cost 8 allocation of resources 6 ambrosia beetle 132 amplification 39, 44 anatomical 33-35, 39-41, 43, 44, 46-51, 55, 56, 61, 64, 65, 67, 68, 243, 245, 247, 248 antibiosis 4, 292, 295 antibiotic effect 110 antifungal properties 36 anti-predator defense 17 antixenosis 4, 292 apical dominance 132 apparency 6, 108, 113, 114, 125, 173 artificial diet 90, 92-97, 199 artificial inoculation 33, 51, 52, 57, 58, 61, 63, 255 artificial larval diet 11 asynchronous attack 48 asynchrony 8, 79, 83, 100, 101, 242 attack behavior 59 attack densities 47, 51, 62

attack failure 109 attack pressure 48 attack rate 107, 108, 111 attack strategy 49 attractant 108, 113, 154, 155, 164, 275 attraction 17, 67, 110, 125 attractive odor 113 axial parenchyma cell 36 bacteria 15, 138 balance between carbon and nutrient availability 6 balance between growth and differentiation 6 bark beetle 6, 13, 14, 16, 31-33, 35-39, 41, 43-45, 47-68, 71, 73, 75, 77, 132, 133, 140, 179, 183, 226, 228, 240, 243-246, 249, 251, 253, 255258 bark beetle attack 13, 14, 31, 32, 38, 41, 43, 44, 48-51, 62, 68, 133, 243, 244, 246, 257 bark beetle attack strategies 31 bark beetle biology 31 bark beetle life cycle 31 bark resin canal 109, 114, 117, 119, 121, 124, 125 bark thickness 32, 109, 115, 121, 123 beetle aggregation 35, 37, 47 beetle behavior 49 beetle colonization strategies 49 beetle establishment 56 beetle galleries 39, 57, 251 beetle maternal galleries 49 beetle success 38, 50 beetle-associated fungi 46, 60 behavior, avoidance 4 behavior, feeding 198, 240 behavior, oviposition 4, 112 behavioral adaptation 5

311

312

KEYWORD INDEX

bioassay 6, 12-14, 52, 64, 83-86, 88, 92, 95, 99, 101, 114, 173, 175, 176, 197, 198 biochemical 5, 6, 12, 44, 45, 99, 109, 121-123, 138, 139, 175, 248, 249, 251 biochemical adaptation 5 biochemical cascade 12 biochemical change 139 biochemical indicator 248, 249 biorational spray 206 biotic 1, 3, 4, 11, 14, 15, 16, 19, 39, 58, 67, 110, 171, 172, 193, 224, 240, 247, 248, 250 biotic agent 14, 171 biotic aggression 39, 240 biotic environment 3 biotic factor 4, 247, 250 biotype 11, 140, 172, 174, 175, 177-183, 195, 196, 204-206 biotype development 177, 179-181 bisabolene 122, 123, 275 blister 33, 35, 43, 58 blue stain 51, 53-55, 58, 63, 64 borer 105, 131-134, 140, 203, 220, 222-224, 227-229, 243, 277, 279, 281, 294, 295, 297-299, 305 borer colonization 133, 223 boring damage 131 boring sawfly 131 boring species 131 bornyl acetate 95 breeding program 66, 67, 108, 123, 124, 177, 190, 194, 245, 247, 252, 267, 295, 302 bud break phenology 84, 85 bud burst 79, 84, 86, 88 bud flush 84, 242 bud phenology 84, 85 budbreak 7, 116 budburst 80, 84, 85, 116, 117 budburst phenology 84, 85 bud-galling 156, 158

cage experiment 114, 115 cambial layer 132 cambium 51, 117, 120, 121, 131, 132, 141, 274, 276, 278 camphene 95, 249, 250, 275 carbohydrate 5, 80, 81, 90, 249, 251, 254, 255, 257 carbon allocation strategies 13, 81 carbon-based defensive chemical 82 carbon-nutrient-balance-theory 253 carene 123, 164, 249, 250, 275 carpenterworm moth 131 cell 2, 12-14, 17, 32, 33, 35-41, 43, 44, 47, 48, 50, 59, 109, 115, 119-121, 124, 133, 134, 139, 140, 141m 154, 251 cell differentiation 121 cell division 36, 40, 41, 43, 47 cell metabolism 37, 47 cell necrosis 38 cell wall 139 cerambycid reproductive behavior 133 cerrado vegetation 143, 144 chalcone synthase 45, 52 chemical 3, 5-8, 12, 13, 19, 32, 34, 35, 37-40, 44-46, 51, 64, 81, 82, 99, 100, 107-110, 113-117, 121-124, 133, 134, 138, 139, 150, 155, 158, 159, 174, 186, 191, 193, 194, 196, 198, 199, 202, 203, 206, 224, 225, 243-245, 248-250, 253, 255, 279, 281, 292, 293, 295, 300, 302, 304, 305 choice experiment 109, 114 citronellol 95 classical breeding 218, 219, 247, 252 clean forestry 253, 256 clearwing moth 131 climate change 106 climate parameter 67 climatic condition 47, 48, 134, 242, 246, 258

KEYWORD INDEX

clonal deployment strategies 191, 194, 196, 208 clone 1, 10, 36, 42, 64, 66, 83-86, 88, 89, 95, 96, 99, 101, 109-111, 114, 115, 117, 137, 157, 170, 171, 173-179 colonization by fungus 50 colonization process 31 colonization strategies 32, 36 Compartmentalization process 41 compensation 2, 80 compensatory feeding 4 compensatory growth 3, 80 compensatory photosynthesis 80, 88, 100, 101 compensatory process 2 complementarity 33, 48 complex interaction 16 condensed tannin 154, 155, 159, 164, 254, 257 confusion 108, 125, 304 conifer shoot 105, 116, 117, 121 constitutive 6, 12, 13, 32, 33, 35, 49, 50, 58, 64, 66, 67, 81, 107109, 114, 117-120, 122, 124, 125, 138, 146, 149, 226, 228, 240, 243-245, 251, 255, 274, 277 constitutive defense 32, 33, 50, 146, 244 constitutive resin 35, 117, 118, 120, 228, 277 constitutive resistance 32, 67, 114, 119, 138, 243, 244, 255 constitutive secondary metabolite 6 containment 139 cooperative strategy 56, 60 cortical resin acid 123 cossid moth 132 crop rotation 193, 196 cross talk 15 cytological 39

313

de novo resin terpenoid formation 121 dead and dying tree 133 deathwatch beetle 132 defense system 31, 33-36, 47-50, 62 defense-related gene 139 defensive chemical 32, 46, 51, 81, 82, 95, 108, 116, 122, 248 defensive compound 81, 95, 100, 101 defensive function 16, 121, 123 defoliator 79-83, 85, 89, 91, 93, 95, 97, 99, 100, 105, 190, 196, 205, 240, 241, 243, 246, 255, 257, 295297 delayed induced resistance 44 delayed induced response 12 delayed resistance 36, 41, 50 density dependent factor 12, 18 density dependent mortality 18 deployment decision-making 177 deployment of tree resistance 170, 189, 265, 267, 269, 271, 273, 275, 277, 279, 281 deployment strategies 182, 189-191, 193, 194, 196, 205, 208 deterrence 46, 67 deterrency 114, 119, 123, 124 deterrent 2, 17, 36, 80-82, 113, 115, 125, 155, 164, 165 detoxification system 5 diet bioassay 83, 92, 101 differentiation 6, 12, 36, 40, 41, 43, 47, 121, 251, 253 digestibility reducer 81 dispersal 7, 80, 11, 112, 114 dispersal behavior 111 dispersal capacity 7 dispersal pattern 112 diterpene 52, 123 diterpene resin acid 123 dose-response function 67, 82-101, 293 Douglas-fir 67, 82-100, 293

314

KEYWORD INDEX

drought 3, 7, 133, 134, 171, 223, 225-227, 253, 255, 256, 258, 292, 297 dynamics of herbivore populations 138 early-season feeder 79, 83 ecological cost 8 ecophysiological 6 ectomycorrhizal 82, 100 egg 4, 13, 17, 57, 59, 60, 80, 81, 109-112, 114, 117, 119-121, 124, 206, 207, 225, 227, 242, 243, 269, 270, 278, 297 elicitor 12, 40, 63, 123 endemic range 134 energetic consideration 51 energetic expenditure 51 energy-demanding process 51 enhancement of resistance 247, 252 enviornmental factors, abiotic 11, 224 environmental conditions 49, 64, 112, 154, 246-249, 252, 258 environmental factor 9, 11, 14-16, 31, 49, 64, 68, 133, 163, 197, 224, 280 environmental factors, biotic 11, 14, 224 environmental gradient 154 environmental variation 154, 163 enzyme 45, 109, 121-123, 139, 251 enzyme activities 39, 52, 62, 123 eucalyptus longhorned borer 133 evolution of conifer defense 49 evolutionary history 4, 224 exhaustion of host defense 50 exhaustion of tree defense 50-52, 55, 56, 58, 63 exotic beetle 67 exotic versus native plantation trees 304

false powderpost beetle 132 farnesene 123 fecundity 4, 13, 18, 19, 85, 137, 138, 201, 225, 226 feeding behavior 198, 240 feeding bioassay 114 feeding deterrency 123, 124 feeding deterrent 36 feeding stimulant 115, 198 feeding tunnel 132 fertilization 64, 100, 169, 28, 229, 253-255 field-testing for resistance 109 fire 133, 292, 296, 304 fitness 12, 16, 17, 84, 85, 92, 95, 196 fitness, insect 18 fitness, plant 3 flood 120, 133, 171 foliage toughness 89 foliar biochemistry 82 foliar terpene 95, 96, 113, 114, 123 folivore 226 food quantity 31 forest pest management 2, 65, 194, 239, 245, 246 forest protection 67, 240 fungal endophyte 100 fungal growth 39, 46 fungal infection 42, 155 fungi 31-33, 35, 38-41, 44, 46, 47, 5060, 63-65, 67, 68, 82, 132, 138, 143, 155, 156, 165, 244, 255, 258, 300 fungistatic effect 39 fungus aggression 40 . fungus inoculation 47, 51, 52, 54, 250, 255 gall 10, 105, 131, 137, 140-142, 144, 147, 156, 164, 241, 256, 266, 269, 270, 281, 300, 305 gall diversity 150 gall induction 138, 141, 143, 149 gall initiation 7, 143, 256

KEYWORD INDEX galler 140 gallery boring 34 gallery initiation 34 gall-forming insect 137, 140, 143 gall-inducing 140, 141 galling 140 galling herbivores 138, 144, 146, 150 galling insect 8, 138, 140, 143, 146, 147, 150, 256 galling population 144 galling sawflies 154, 155, 158, 164 galling species 141, 144 galling-agent 140 gene activation 32, 39, 45, 47 gene expression 123, 200, 268 gene transcription 32 generalist 15, 17, 19, 20, 153, 155, 156, 164, 176, 177, 298 genetic difference 83, 163, 244 genetic diversity 169, 173, 180, 182, 219, 229, 247, 248, 253, 258, 293 genetic engineering 172, 178, 179, 190, 194, 199, 204, 218, 219, 245, 251, 252 genetic factor 64, 154 genetic improvement program 172, 173, 177, 183, genetic marker 251 genetic re-arrangement 153, 165 genetic resistance 106, 111, 190?, 173, 246, 247 genotype by environment interaction 258 geographic distribution 67, 134 ghost moth 131 glandular exudate 7 glandular trichome 7 growth 3-9, 12, 16, 19, 39, 45, 46, 57, 68, 80-90, 92-97, 100, 101, 116-118, 125, 132, 137, 140, 157, 158, 165, 169, 183, 190,

315

192, 196, 199-202, 206, 218, 220, 221, 243, 251, 253-258, 266, 268, 276, 279, 287, 288, 292=301, 303, 306 growth and defense 8, 257 growth rate 16, 19, 68, 80-82, 86, 88, 101, 137, 138, 196, 200, 202, 266, 287, 293, 295, 297-299 growth-differentiation-balance-theory 253 guild defence 108 hairs 7, 141 half-sib seedling 83, 87, 100, 101 healthy host 132 heartwood 45 herbivore response 154, 156, 160-162 herbivore-induced volatile emission 17 heritable trait 84 histological 39, 40, 42-44, 48, 138 horizontal galleries 34, 49, 59 horntail 131 host acceptance 4 host choice 154 host plant phenology 80 host plant specialization 5, 17 host range 4, 164 host shift 153 host-driven mortality factor 144, 146 host-selection behavior 111 hybrid 107, 153-165, 183, 190, 191, 197-200, 203, 204 hybrid chemistry 164 hybrid heterosis 155 hybrid susceptibility 155 hybrid zone 153 hybridization 107, 153, 154, 183, 198, 203, 204, 218, 219, 251, 265, 266268, 275, 276 hypersensitive reaction 36-41, 44-46, 48, 49 hypersensitivity 137, 140, 146, 149

316

KEYWORD INDEX

hypersensitive response 12, 14, 34, 40, 47, 48 inactivation 139 indirect defense 17 individual strategy 59 Induced 12-14, 16, 17, 32, 37-40, 43, 44, 51, 55, 58, 117, 121, 123, 124, 138, 142, 144, 145, 147, 198, 240, 244, 250, 256, 273, 275, 280 induced defense 32-34, 36, 37, 41, 43, 47-49, 64, 81, 99-101, 124, 125, 133, 137, 244, 245, 255, 274-276 induced plant response 12 induced protection 41-44 induced reaction 12, 43, 44, 62, 134, 244, 245 induced resin flow 34, 36, 37, 40, 44-47, 52, 58 induced resistance 6, 12-15, 17, 32, 44, 61, 67, 81, 99, 137-139, 143, 149-151 induced response 12, 41, 45, 48, 56, 124, 134, 137 induced susceptibility 12, 41,45, 48, 56, 124, 134, 137 induced synthesis 34 induced trait 146 inducible plant defense 108 inducible resistance system 146 inducible strategy 147, 149 inducing agent 138 induction 1, 6, 12-15, 17, 18, 39, 43,44, 99, 101, 114, 138, 141, 143, 149, 279 inheritance pattern 154-156, 159, 164 inhibitory effect 46 inoculation 13, 33, 39, 42, 43, 47, 51-53, 57, 58, 60, 61, 100 inoculation density 51, 61, 63, 65

insect adaptation 124 insect behavior 4, 111, 201 insect bioassay 12 insect emergence 80 insect fecundity 225 insect fitness 17, 18 insect growth 4, 5, 8, 16, 90 insect life history 7, 12, 18 insect outbreak 1, 16, 19, 225, 292 insect performance 4, 5, 13, 15, 16, 19, 225, 228, 243, 256 insect pest management 1 insect population dynamics 12, 15, 16, 19 insect preference 4 insect resistance 1, 173, 177, 180, 181, 183, 196, 202, 205, 208, 218-220, 225, 226, 228, 229, 252, 268 insect resistant germplasm 218, 219, 229 insect response 2, 9, 11, 15, 90, 178 insect survival 202 insect-induced resistance 12 insect-resistant plant 1, 9 integrated pest management 1, 68, 189, 295, 300, 303-306 intercellular communication 39 intermediate plant 149 interspecific hybridisation 153, 154 interspecific tree hybridization 183 interspecific variation 3, 34, 222, 223 intra-specific variability 66 intraspecific variation 11, 154 invader 32, 138, 139 irrigation 190, 253, 255, 256, 270 isoprenoid 122 jasmonate 123 juvabione-type terpenoid 122 key nutrient 90 key-factor 31 kino 133, 134

KEYWORD INDEX

larval chemical defense 19 larval defense 18 larval growth 80, 199 larval predation 18 larval survival 18, 195, 202, 243, 298 latex 107 leader kill 110, 111 leader silhouette 113 leafbeetle 7, 17, 154, 156, 158-165, 222, 226, 228 leaf gall 141, 142, 156, 158, 160, 161 leaf toughness 9, 81, 292 leaf-beetle 154, 156, 158, 160, 161 leaf-folding 156 leaf-galling 156, 158, 160, 161 lethal density 42 levopimaric acid 123 life history trait 5, 7, 9, 18 life table 109, 146 lignin 33, 133, 136 lignin stone cell 133 limonene 46, 95, 123, 2751 linalool 95 localization 139 localized resistance 138 long term response 36 longhorned or roundheaded borer 132, 133 long-term induced response 41 long-term inducible response 36, 41 magnesium 94, 296 mass attack 48, 54, 55, 60, 256 mass inoculation 42, 43, 53, 54, 58, 60, 251 mass screening 108 mechanical stress 39 mechanical trait 138 mechanical wound 13, 14, 39, 43, 58, 123

317

mechanism of resistance 2, 3, 66, 79, 82, 84, 85, 88, 89, 95, 99, 105, 118, 178, 179, 240, 277,278, 306 mechanisms of attack 32, 50 Mediterranean climate 134 meristematic tissue 132, 140 metabolic activities 51, 57 metabolic modification 40 metabolism of cells 36, 37 metallic or flatheaded borer 132 microbial mutualist 82, 99-101 microcapsule 95 microorganism 3, 4, 12, 13, 138, 139, 244 miner 105, 140, 203, 221, 222 mineral 81, 83, 90, 91, 100 minimum threshold 155 models of tree resistance 2 modification of resistance 224 moisture availability 134 molecular biology technique 14 monoterpene 33, 40, 45, 46, 52, 57, 644, 83, 95, 96, 98, 99, 101, 120, 228, 255 morphological changes 13 mortality 7, 16-18, 52, 80, 109, 117, 134, 140, 143, 144, 146, 148, 178, 192, 197, 201, 203, 204, 207, 223, 224, 243, 246, 247, 251, 258, 271, 277, 279, 292, 296, 297, 300, 301 mortality pressure 146 multicomponent resistance index 123, 124 multiple pest screening 205 multitrophic defence system 108 multitrophic plant insect interaction 122 mycorrhizae 82, 100, 101 myrcene 95, 123, 275 natural enemies 5, 9, 16, 17, 80, 82, 100, 101, 137, 143, 144, 146, 148,

318

KEYWORD INDEX

156, 179, 193, 207, 227, 244, 253, 255, 256, 258, 292, 303, 305 natural enemy-driven 146 necrosis 38, 140, 273, 274 necrotic response 139 necrotic tissue 14, 140 needle resin 18, 19 needle toughness 80, 88 nematode 138, 266, 271-275 neosynthesis 45 nitrogen 5, 9, 64, 80, 82, 83, 90, 198, 227, 228, 245, 253-255, 279, 295, 301 no-choice experiment 109, 114 non-outbreak population 48, 65 nonpathogenic stimuli 138 non-target organism 195, 206 nutrient 5, 6, 12, 39, 46, 81-83, 90, 99, 139, 157, 190, 225, 227, 228, 246, 253, 254, 257, 293, 295 nutrition 108, 138, 150, 279 nutritional niche 83 nutritional status 81 nutritive quality 81, 89, 100, 101 oleoresin 35, 95, 133 oleoresin exudation pressure 35 olfactory or gustatory stimuli 114 ontogenetic 5, 81 ontogeny 8 opportunity cost 8 optimality 6 outbreak population 48, 65, 66 outer bark 33, 35, 132, 134, 278, 280, 281 oviposition 4, 6, 10, 39, 52, 55, 81, 109-114, 116, 117, 119, 120, 123-125, 147, 155, 164, 197-199, 206, 292 oviposition behavior 112 oviposition deterrency 119, 123 oviposition repellency 110 oxidative 139

palatability 154, 155, 157 parasitic fungi 155-157, 165 parent host plant 153, 156 parental species 153-157, 159, 302 pathogen 4, 12, 13, 31, 41, 42, 53, 55, 57-62, 65, 82, 100, 122, 123, 132, 133, 138, 139, 144, 146, 148, 150 pathogenic fungi 51, 53, 55, 57, 59, 60, 132, 258 pathogenic fungus 13, 42, 55, 57, 59, 60, 62 peptide 139 performance of the insect 14, 18 pest biotype evolution 175, 181 phasmid 79 phenol 33, 36, 39, 40, 44-47, 50-52, 64, 125, 243, 275, 300 phenolic 5, 6, 36, 38, 40 phenolic compound 38, 39, 64, 164, 243, 251 phenolic glucoside 154, 155, 157, 164, 198, 199, 202, 203, 205 phenolic secondary metabolite 154 phenological asynchrony 83, 100, 101, 242 phenological defence 116 phenological development 116 phenological resistance 117, 242, 295 phenological stage 108 phenology 4, 7, 8, 80, 83-86, 88, 108, 116, 117, 124, 125, 157, 158, 242, 293, 295 phenotypic plasticity 14, 16 phenotypic response 12, 225, 246 pheromone 35, 37, 50, 56-60, 65 phloem 16, 33-36, 38, 39, 45, 47, 5052, 54-56, 58, 62, 63, 66, 105, 119, 120, 124, 132, 141, 240, 241, 243, 244, 248-251, 279 phloem colonization 50, 62 phloem parenchyma cell 33, 40, 43, 44, 243 phloem reaction zone 40, 49, 52, 244

KEYWORD INDEX

phloem tissue 132, 222 phosphorus 82, 94, 296 photoperiod 106 physical factor 4, 7, 133, 134, 198 physiological condition 132, 133 physiological process 50, 274 phytoalexin 139 phytocentric hypotheses 12 phytopathogenic fungi 31, 57 phytophagous insect 36, 198 pinene 95, 123, 244, 275 pinocembrin 46, 248, 250, 275 pinosylvin 45, 46, 248, 250, 275 pinosylvine methyl transferase 45 pioneer beetle 57 plant apparency 6, 113 plant breeding 2 plant form 132 plant gall 140 plant genotype 2, 9, 18 plant nutrition 138, 146, 150 plant pathologist 138 plant phenology 8, 80, 116 plant phenotype 3 plant quality hypothesis 253, 254 plant trait 2-4, 6, 9,, 11, 13, 15-19, 82, 155, 164 plant/insect interaction 2, 11, 14 plantation strategies 191 plant-driven 144, 146 plasmodesmata 39 plastic response 14 pollinator 9 polygenetic resistance 111 polymorphism 9, 10 polyphenolic compound 3, 139 polyphenolic parenchyma cell 13, 35, 36, 251 polyphenolic resin 133 polyphenolic substance 141 population dynamics 12, 15, 18, 19, 31, 38, 43, 93, 95-97, 224, 227, 229, 258

319

population growth 19, 85, 92-94 population outbreak 269 population strategy 56, 108 positive feedback loop 82 potassium 94 powderpost beetle 132 precursory compound 32 preference 4, 11, 100, 112, 114, 137, 138, 157, 164, 176, 197-199, 243, 304 preference test 156-161, 165 preformed 32, 34 preformed defense 32, 36 preformed induced defense 32-34, 37 preformed resin 34, 35, 37, 38 preformed resistance mechanism 32 preformed response 48 prenyltransferases 121 primary metabolite 4, 5, 81, 90 primary resistance 133 progeny trial 107 protein 8, 12, 81, 90, 139, 154, 268, 296 proteinase inhibitor 195, 199, 200, 201, 208 pure individual 153 radial growth 86, 87, 118, 257 rapid aggregation 50 rapid induced resistance 14 rapid induced response 12 rapid tree response 47 ray parenchyma cell 39 reaction mechanism 38 reaction tissue 46 reaction zone 39-41, 45-47, 51, 52, 244, 258, 250, 255 reductive 139 refugia 179-182, 202, 208 repellency 110, 114, 123-125 repellent 35, 46, 106, 108, 113, 125, 154, 155, 274-276

320

KEYWORD INDEX

resin 33-35, 38-40, 43, 46, 48, 50, 55, 57, 59-61, 108, 109, 115, 116, 120, 122, 124, 125, 133, 226, 243, 244, 248, 255, 279, 280, 293 resin acid 18, 19, 33, 45, 120, 123, 254 resin canal 107, 109, 114, 115, 117125, 276 resin crystallization 35 resin duct 13, 33-35, 37, 39, 41-45, 48, 49, 56, 58, 59, 123, 243-245, 274, 277, 279, 280 resin flow 33-35, 37, 38, 40, 44-50, 52, 58, 59, 122, 228, 254, 255, 277, 279, 281 resin impregnated zone 55, 62 resin network 34 resin pocket 35, 58 resin system 33 resin translocation 37 resistance 1-5, 7-18, 20, 31, 32, 3436, 42-45, 47, 48, 50, 51, 53-59, 61, 62, 65-68, 79-84, 87-89, 96, 99, 100, 106, 107, 109-112, 114, 115, 117-119, 123-125, 133, 134, 137-140, 143, 144, 146, 149, 150, 153-155, 158, 159, 162, 165, 169-183, 189, 190, 192196, 199-206, 208, 217-220, 223229, 239, 240, 242-258, 265, 268-274, 276-281, 287, 292-305 resistance against insects 1, 7, 13, 14, 18, 66, 67, 105, 122, 137 resistance gene 12, 14, 199, 254, 269, 271 resistance gene pool 107 resistance mechanism 2, 3, 9, 11, 31, 32, 38, 41, 64-68, 79, 81, 83, 84, 88, 95, 99, 105, 108, 109, 114, 115, 118, 124, 125, 133, 134, 138, 144, 146, 171, 172, 174-176, 178-183, 189, 195, 204,

205, 208, 240, 244, 245, 247, 277, 278, 281, 298, 305 resistance of conifers to bark beetles 31, 38, 65, 66, 243 resistance trait 3, 4, 6, 7, 9, 11, 12, 1419, 81, 82, 159, 165, 169, 172, 180, 208, 224, 229 resistance, genetically determined 4, 243, 249 resistance-screening program 106, 177 resistant 1, 2, 4, 8, 12, 15, 16, 36, 42, 56, 59, 80, 82-101, 109, 112-124, 139, 146, 149, 154-156, 160, 161, 174, 176, 179-181, 183, 189, 192, 193, 196, 202, 204-206, 217-220, 222, 224, 226, 228, 229, 243, 244, 246-249, 251, 252, 255, 265, 266, 268, 269-281, 287, 292-306 resistant genotype 10, 110 resistant plant 1, 2, 4, 9, 14, 16 resource availability 6 rust fungi 155, 165 sapwood 33, 34, 38, 41, 51, 53-56, 58, 61-63, 244, 251, 278, 280 sapwood invasion 53, 58, 63 sapwood occlusion 50, 53-55, 63 sawflies 79-81, 154-156, 158, 164, 203, 228 screening for resistance 107, 175, 219 scribble-barked gums 132 secondarily invading scavenger 133 secondary chemistry 133, 138, 153, 154 secondary compound 6, 11, 146, 154, 155, 164, 175, 198, 274, 275, 295 secondary metabolite 4-7, 9, 11, 17, 19, 33, 47, 48, 51, 52, 57, 64, 66, 81, 122, 164, 224, 225, 227, 228, 248 secondary reaction 38 secretory cell 32, 33 secretory structure 32

KEYWORD INDEX

selection pressure 118, 165, 252 selective pressure 66, 153, 172, 175, 178-181, 208 sesquiterpene 52 sesquiterpenoid 122 shoot growth 84, 116, 255 shoot infesting insect 105, 124 short term response 36 short-rotation woody crop 190, 191 short-term inducible response 36 sieve cell 35, 39 signal compound 12 simultaneous attack 50, 56 sink/source regulation 6 Sitka spruce 33, 106, 107, 109, 111, 113-116, 118-120, 122, 124 slow growth-high mortality 16 solitary strategy 59 soluble phenol 33, 36 spatial distribution 112 specialist 6, 15, 132, 153-156, 176, 302 specialized insect 9, 17, 176 spore 52, 61, 63, 65 spruce budworm 80-101, 105, 116, 180 staining fungi 53 starch 254, 257 starvation 80, 114 stem gall 142 stilbene aglycons 46 stilbene syntase 45, 52, 270, 275 stimulation 37, 44, 45, 51, 52, 55, 58, 62, 63, 80, 245 stone cell mass 33, 59 stress effects on insect resistance 226 stress experiment 16 stress hypothesis 16, 225 stress response 16 stress, abiotic 19, 171, 172, 224 stress, biotic 19, 171, 172, 224 stressed host plant 132

321

stressed plant 16, 229, 253 stressed tree 16, 134, 225-227, 229, 256, 292 structural constitutive defence 109 sub-lethal effect 4, 16 successful colonization 31 sugar 38, 45, 82, 83, 92-95, 226, 254 survival 4, 5, 7, 9, 10, 16, 18, 19, 81, 83-85, 90, 95, 133, 134, 137, 138, 157, 165, 195, 202, 223-225, 228, 243, 298, 303 susceptible 31, 36, 42, 51, 68, 83-96, 98, 100, 109, 119, 120, 134, 149, 165, 178, 190, 192, 204-206, 224227, 229, 246, 249, 251, 252, 255, 256, 265, 266, 271, 273, 275, 277, 293, 294, 296-299, 301-305 susceptible genotype 10, 114, 249, 300 susceptible plant 4, 16, 112, 149 synchrony 8, 79, 86, 117, 125 synergistic interaction 11 synthetic hypothesis 38 synthetic pathway 45 systemic 12, 138, 240, 245, 279 systemic induced defense 245 systemic induction of resistance 43 systemic resistance 138 tannin 6, 8, 154, 155, 159, 164, 202, 249, 254, 257, 288, 295, 300, 302 temperature 67, 106, 112, 206, 246, 304 temporal variation 112 temporal window 9 terpene 35, 38-40, 44-47, 51, 52, 55, 64, 83, 95, 96, 98, 109, 113, 114, 123, 228, 243, 244, 249, 255, 273, 274 terpene synthase 45, 121 terpenoid 5, 6, 18, 121-125, 133 terpenoid synthase gene 123 thick bark 3 third trophic level 17, 258

322

KEYWORD INDEX

thorn 107 three-trophic-level interaction 82, 83, 100, 101 threshold of attack density 50, 51, 56, 61-63, 65, 66, 251 threshold response 154 timber beetle 132 timber worm 132 tip moth 131, 228 tissue restoration 42-44 tolerance 2, 3, 6, 57, 59, 80, 86, 100, 101, 134, 137, 171, 172, 174, 178, 208, 225, 266, 268, 276, 292, 295, 298, 299, 302 tough leaves 7, 80 tough needle 80, 101 toughness 7, 9, 80, 81, 88, 89, 100, 101, 292 toxic 35, 46, 47, 108, 122, 124, 195, 200, 202, 244, 268 toxic chemical 3, 5, 202 toxic effect 154, 243 toxic metabolite 139 toxicity 46, 110, 115, 119, 125, 194, 200, 202 toxin 2, 50, 54, 63, 81, 195, 200202, 206, 252, 266, 268, 275 trade-off 8, 9 transduction 139, 270 transformation technique 14 transformed woody plant 14 transgenic Bt 200, 201 transgenic poplar 266, 268 transgenic tree 14, 195, 201, 219, 252 translocation 37, 39 transversal galleries 58 traumatic resin 108, 109, 114, 115, 117, 120-124, 279, 281 traumatic resin duct 13, 41-45, 48, 56, 59, 244, 245, 277, 279-281 traumatic resinosis response 121 tree death 50, 52-55, 58, 59, 63

tree defense strategies 49 tree genetic factor 64 tree killing 183 tree phenology 108, 116 tree recovery 80 tree resistance 1, 2, 16, 20, 32, 34, 35, 38, 43, 45, 47, 50, 51, 53-59, 61, 6468, 80, 82, 88, 111, 131, 134, 169171, 176, 178, 189, 190, 226-229, 239, 240, 245-249, 251, 253, 254, 256-258, 265, 270, 272, 277, 290, 281, 300 tree response 36, 43, 44, 47-49, 52, 56, 248, 250 tree strategy 48 tree vigor 80, 86, 100, 225, 228, 229, 251, 254, 255, 258, 306 tree/insect interaction 18, 82, 100 trichome 3, 7, 9, 107 tri-trophic interaction 18, 82, 100 tri-trophic level effect 16 trophic relationship 116 tropical forestry plantation species 294 tunnelling insect 58 tussock moth 79, 277 twig borer 131, 203, 277 undifferentiated tissue 7 unsuitable food 137 vapor 46, 48 vertical galleries 34, 49, 57 vertical resin duct 49, 255 vigor gradient 57 virulence gene 12 virus 138 volatile 17, 18, 108 volatile chemical 134 volatile compound 17 volatile induction 17, 18 volatile terpenoid 122, 123 walking stick 79

KEYWORD INDEX water stress 64, 134, 226, 227, 250, 255 water stressed tree 134, 226 weevil 105-115, 117-121, 124, 125, 132, 206, 222, 226, 228, 240, 243, 297, 305 western spruce budworm 82-85, 87101 white pine weevil 105-109, 115, 117, 119—121, 124, 125, 226, 228 white spruce 43, 80, 106, 107, 111, 113, 117-120 willow 7, 10, 17, 153-158, 164, 165, 174, 182, 192, 193, 265 winding galleries 49, 58 window of susceptibility 80, 124 within-plant resistance 112 within-plant variation 112 wood boring life history strategies 131 wood wasp 131, 133 wood-boring insect 131, 132, 266 wound periderm 40-44, 274 wound reaction 39, 40, 42, 44 wound response 44, 109 wounding 13, 14, 33, 36, 37, 39, 40, 42-44, 47, 51, 52, 58, 62, 108, 120-122, 244 xylem resin canal 117, 120-123 xylem tissue 132 xylophagous insect 49, 245 young larvae 105, 109, 117, 124, 277, 280, 281 zinc 94

323

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Species Index

Batocera horsfieldi 265, 268, 269 Batocera lineolata 265, 268 Bauhinia brevipes Vog. 138, 140, 141, 142, 144, 147, 149 Betula 157, 164, 220 Betula pubescens 13 Betula maximowiczinana 223, 224 Betula nigra 223, 224 Betula papyrifera 223, 224 Betula pendula 222, 223, 233 Betula platyphylla 224 Betula platyphylla var. japonica 223 Betula platyphylla var. szechuanica 223 Betula populifolia 224 Betula populifolia Whitepire 223 Betula pubescens 223 Betula spp. 222 Bignoniacaea 143 Bostrichidae 132 Bowdichia virgilioidis 143, 144 Brachyderes incanus 241 Brentidae 132 Bupalus piniarus 13, 258 Buprestidae 132 Bursaphelenchus xylophilus 266, 271 Byrsonima verbascifolia 143, 144

Abies 35,43,58, 119 Abies concolor 35 Acacia 182, 88, 289, 299, 306 Acacia crassicarpa 299 Acacia mangium 298, 299 Acacia mearnsii 288 Acacia Senegal 288 Acacia spp. 220 Acer 220 Acer freemanii 220 Acer rubrum 220 Acer saccharum 226 Adelges abietis 241, 242, 245 Adelges laricis 251 Adelges picae Ratzeburg 41 Adelges piceae 183 Adelges tsugae 183 Agonoxenidae 131 Agrilus anxius 220, 222 Agrilus sexsignatus 298 Agrobacterium 252 Agrobacterium tumefaciens 201, 268, 298 Alsophilia pometaria 221 Anaglyptus subfasciatus 277 Anisota senatoria 221 Annona coriaceae 143 Annonaceae 143 Anobiidae 132 Anoplognathus porosus 302 Apocheimia cinerarius 265 Apochina cinerarius 268 Apocynaceae 143 Apriona japonica 265, 299 Arabidopsis thaliana 14 Argyresthia cupresssella 221, 222 Argyresthiidae 131 Aspidosperma tomentosum 143 Asteraceae 143 Atta sexdens rubropilosa 304 Australes 270

Cupressus arizonica 299 Cupressus funebris 299 Cupressus. torulosa 299 Calliteara argentata 277 Casuarina 288 Cecidomyiidae 138, 141-144, 156, 277 Cedrela odorata L. 294, 295 Cedrus 35, 119 Cedrus atlantica 67 Cephalcia abietis 241 Cephidae 131 Cerambycidae 132-134, 277, 296 Ceratocystis polonica 244, 249, 250, 251 Chaitophorus poplicola 226

Baccharis dracunculifolia 143 Bacillus thuringensis 195, 252, 304 325

326

SPECIES INDEX

Choristoneura 79 Choristoneura conflictana 202 Choristoneura fumiferana 80 Choristoneura fumiferana Clem. 180 Choristoneura occidentalis 82 Choristoneura spp. 105, 116 Chrysomela populi 200 Chrysomela scripta F. 193, 194, 195, 196, 197, 198, 199, 200, 201, 203, 205-207 Chrysomelidae 156-158, 193, 200 Cinara cupressi 294, 299 Clethrionomys rufocanus 266, 272 Cocos 288 Coffea arabica 304 Coffea robusta 304 Coleoptera 79, 105, 131, 133, 134, 141, 142, 157, 193, 200, 277, 296, 298, 299, 302 Combretaceae 143, 144 Contarinia 144, 147, 149 Contarinia sp. 138, 141, 142 Contortae 271 Coptotermes curvignathus 299 Cornus 220 Cornus florida 227 Corythucha cydoniae 220, 221 Cossidae 131 Cotoneaster 220 Crepidodera fulvicornis Fabr. 156, 158 Cronartium quercuum Berk. 177 Cronartium rubicola 43 Cryphonectria cubensis 183 Cryptococcus fagisuga 242, 257 Cryptomeria japonica 266, 277 Cupressocyparis leylandii 299 Cupressus 306 Cupressus lusinatica 294, 299 Curculionidae l41, 142, 297 Cylindrocopturus 105

Dalbergia sisso 288 Danaidae 195 Danaus plexippus L. 195 Dasineura marginemtorquens 10 Dasineura rosaria 158, 165 Davilla regusa 143 Dendroctonus brevicomis 57 Dendroctonus frontalis 34, 49, 53, 58, 183 Dendroctonus micans 33, 34, 49, 50, 53, 59, 60 Dendroctonus pondorosae 35, 44, 49, 50, 53, 57 Dendroctonus punctatus 53, 59, 60 Dendroctonus terebrans 60 Dendroctonus valens 60 Diaphnocoris chlorionis 221 Dilleniaceae 143 Dioryctria 296 Dioryctria spp. 296 Dioryctria sylvestrella 241, 243, 249, 250 Diprion pini 241, 243, 244, 245, 247, 249, 250 Diprionidae 79 Diptera 79, 131, 144, 148, 141, 142, 277 Dothideales 204 Elatobium abietinum 242, 243, 251 Empoasca fabae 220 Epinotia granitalis 277 Epinotia tedella 256 Epirrita autumnata 13 Eucallipterus tilliae 222 Eucaluptus camaldulensis 297, 298 Eucaluptus deglupta 298 Eucaluptus grandis x E. urophylla 298, 299, 303 Eucalyptus 133, 134, 181-183, 190, 227, 287-289, 297, 306 Eucalyptus amygdalina 302 Eucalyptus blaklyi 7

SPECIES INDEX Eucalyptus grandis 298, 302, 303 Eucalyptus haemastoma 132 Eucalyptus japonicus 277 Eucalyptus risdonii 302 Eucalyptus tereticornus 297 Eucalyptus urophylla 298, 302 Eucosma tedella 241 Euonymus spp. 221 Eurosta 140 Eutectona machaeralis 296 Fagus sylvatica 144, 239, 241, 257 Fraxinus pennsylvanica 227 Galerucella lineola 154 Galerucinae 157 Gaylussacia 182 Gelechiidae 131 Geometridae 141, 297 Gilpinia hercyniae 241,256 Gleditsia triacanthos 221 Gmelina arborea 288, 289 Goniptera scutellanus 297 Graellsia isabellae 244, 247 Gympsonoma hiambachiana 203, 204 Halticinae 156, 158 Hamameliste spinosus 220 Hartigiola anulipes Htg. 144 Heliothis 11 Helopeltis spp. 299 Hempitera 299 Hepialidae 131, 132 Heteropsylla cubana 301 Heteropsylla cubana Crawford 294 Hevea 288 Hevea braziliensis 304 Homadaula anisocentra 221 Homoptera 294, 301 Hyadaphis tataricae 221 Hyblaea puera 295, 296 Hylobius abietis 241, 243, 249, 250

327

Hymenoptera 131, 156, 207 Hypsipyla 294, 295, 306 Hypsipyla grandella Zeller 294 Hypsipyla robusta Moore 294 Ilex spp. 221 Imperata cylindrica 299 Ips 35, 49 Ips acuminatus 33, 57, 60, 241 Ips cembrae 62 Ips pini 47 Ips sexdentatus 44, 69, 62, 241 Ips typographus 35, 42, 49, 54, 57, 60-62, 240, 241, 244, 246, 249 Isoptera 299 Iteomyia capreae 158 Juniperus spp. 221 Khaya ivorensis 294 Khaya myasica 294 Khaya senegalensis 294 Khaya spp. 294 Larix 3, 57, 119, 243 Larix decidua 245, 252 Larix eurolepsis (Larix decidua x Larix leptolepsis) 276 Larix gmelini var. japonica 276 Larix gmelini var. japonica x L.leptolepsis 276 Larix leptolepsis 276 Larix occidentalis 34 Larix spp. 265 Lasiocampidae 202 Leguminosae 138, 143, 144 Lepidoptera 79, 131, 132, 141, 142, 193, 195, 202, 203, 277, 296, 297 Leptographium 57 Leptographium wingfieldii 52, 57, 58, 60, 61, 63, 248, 250, 251 Leptographium yunnanesis 57 Leucaena 301, 306

328

SPECIES INDEX

Leucaena collinsii 301 Leucaena diversifolia 301, 302 Leucaena leucocephala 294, 301, 302 Leucaena leucophala x L. diversifolia 301 Leucaena pallida 302 Leucopholis irrorata 298 Liquidambar 182, 190 Liquidambar styraciflua 219 Lochmaea caprea 154, 157, 164 Lochmaea caprea L. 157 Lochmeae 157 Loganiaceae 143 Lonicera spp. 221 Lyctidae 132 Lygaeonematus abietinus 242 Lymantria dispar 79, 193, 202, 203, 219-222, 240, 241, 244, 265, 268 Lymantria monacha 241, 242, 254, 257 Lymexylidae 79, 132, 193 Magdalis 105 Malacasoma americanum 221 Malacasoma disstria Hübner 202, 203, 205 Malpighiaceae 143, 144 Malus spp. 221 Matsucoccus feytaudi Duc. 240 Matsucoccus feytaudii 242, 243 Melampsora 204, 208 Melampsora spp. 174 Melampsora larici-populina 248 Melampsora medusae Thuem. 204 Melampsoraceae 204 Melamspora sp. 155, 156-159, 163, 165 Melasoma populi 252 Melicia regia 300 Mikolia fagi Htg. 144 Milicia 300, 301, 305 Milicia excelsa 300

Miridae 299 Momphidae 131 Monochamus alternartus 270 Morus alba 226 Naupactus lar 141, 142 Neodiprion sertifer 241 Neodiprion autumnalis 81 Neodiprion fulviceps 80 Neodiprion sertifer 18, 19 Neodipron 79 Neophasia menapia 79 Nepticulidae 131 Nicotiana attenuata 17 Noctuidae 131, 296 Ochniceae 143, 144 Oocarpae 270 Ophiostoma 46, 53, 64 Ophiostoma brunneo-ciliatum 60, 61 Ophiostoma ips 60 Ophiostoma novo-ulmi 183 Ophiostoma polonica (cum) 42 Ophiostoma polonicum 51, 60, 61, 255 Ormograptis scribula 132 Orseolia oryzae 140 Orthoptera 79 Otiorhynchus sulcatus 222 Ouratea floribunda 143, 144 P. P. P. P.

euramericana 267 hondurensis 296 pyrameidalis x P. cathayana 267 simonii x (P. pyramidalis + Salix matsudana) 267 P. simoniix P. nigra 267 P. simoniix P. nigra var. italica 267 P. tomentosa var. henan 267 P. tomentosa var. jiangan 267 P. tomentosa var. jieye 267 P. tomentosa var. jinxi 267 P. tomentosa var. taxin 267

SPECIES INDEX

P. tomentosa var. xiaoye 267 P. tomentosa var. yixian 267 P. virginiana 270 P. yunnanenis 49 Pailga machoeralis 296 Panthomorus sp. 141, 142 Paraserianthes falcataria 288 Paropsis atomaria 7 Paulownia 182 Phasmida 79 Phellinus weirii 43 Phoracantha semipunctata 296 Phoracantha semipunctata F. 133, 134 Phratora vitellinae 17, 155 Phratora vulgatissima 154, 193 Phyllaphis fagi 242 Phyllocolpa 156 Phyllotachys 182 Phylloxera vastatrix 140 Phytolyma lata 300, 305 Picea 33, 57, 119, 243 Picea abies 13, 33, 34, 35, 36, 42, 239-241, 244, 245, 248, 249, 250, 251, 254, 255, 256, 257 Picea abies L. Karst 120 Picea glauca 43, 80, 106 Picea sitchensis 106, 243, 251 Picea spp. 105 Pieridae 79 Pinus 5, 33, 57, 190, 243, 288, 289, 304 Pinus nigra var. therestig x P. simonii 267 Pinus nigra x P. maximowiczii 203 Pinus spp. 105 Pinus banksiana 47, 228, 272 Pinus bungeana 272 Pinus caribaea 296, 298, 301 Pinus caribaea subsp. Hondurensis 296 Pinus caribaea var. bahamensis 296

329

Pinus contorta 35, 44, 47, 50, 246, 249, 272 Pinus densiflora 266, 270, 271, 276 Pinus densiflora 272, 274, 275, 276 Pinus edulis 82 Pinus eliotti 251, 272 Pinus engelmannii 272 Pinus engelmannii Parry ex. Engelm. 107 Pinus exelsa 272 Pinus greggii 272 Pinus khasya 272 Pinus koraiensii 272 Pinus leiophylla 272 Pinus massoniana 272 Pinus merkusii 296, 304 Pinus michoacana 272 Pinus monticola 43, 272 Pinus mugo 273 Pinus muricata 272 Pinus nigra 273 Pinus oocarpa 272 Pinus palustris 272 Pinus patula 288, 296 Pinus pentaphylla 272 Pinus pinaster 240, 241, 243, 249, 250, 273 Pinus pondorosae 80, 249, 270 Pinus pseudostrobus 272 Pinus radiatus 272 Pinus radii D. Don 181 Pinus resinosa 47, 272 Pinus rigida 266, 270, 272 Pinus rigida x P. taeda 266 Pinus rigi-taeda 266 Pinus rudis 272 Pinus spp. 250, 265 Pinus strobes 272, 275 Pinus strobiformis 272 Pinus strobus L. 106 Pinus sylvestris 5, 19, 35, 38, 44, 54, 228, 239-241, 243, 245, 248-250, 254, 255, 257, 273

330

SPECIES INDEX

Pinus tabulaeformis 272 Pinus taeda 37, 53, 58, 226, 266, 272, 274 Pinus taeda L. 180 Pinus taiwanensis 272 Pinus thunbergii 266, 270, 271 Pinus thunbergii 272, 274, 275 Pinus thunbergii x P. densiflora 276 Pinus thunbergii x P. massoniana 275 Pinus yunnanensis 272 Pinus. thunbergii x P. masoniana 266 Pissodes 105 Pissodes harcynae 241 Pissodes notatus 241 Pissodes strobi 43, 109, 111, 113, 114, 115, 117-119, 120, 124, 226, 245 Pissodes strobi Peck 105 Pissodes strobus 226 Pityogenes chalcographus 32 Plagiodera versicolora 155, 226 Plagiodera versicolora Laicharting 200 Platanus 190 Platypodidae 132 Pondorosae 20 Pontania 156 Pontania bridgmanii 158, 164, 165 Pontania pedunculi 158, 164 Popillia japonica 220-222 Populus 157, 164, 182, 189, 190, 193-207, 219 Populus deltoides 197, 198, 203, 226 Populus nigra 252, 268 Populus alba 197, 200 Populus alba x P. grandidentata 199 Populus alba x P. grandulosa 266 Populus deltoides 203, 267, 268 Populus deltoides x P. deltoides 203

Populus deltoides x P. maximowiczii 203 Populus deltoides x P. nigra 197 Populus deltoides x P. nigra 198, 200, 203 Populus tremula x P. tremuloides 198, 200 Populus tremuloides 174, 182, 198, 226 Populus trichocarpa 197 Pristiphora abietina 241, 251 Prosapia bicincta 221 Pseudaulacaspis pentagona 225 Pseudoacacia 182 Pseudotsuga 33, 119 Pseudotsuga menziesii 43, 67, 293, 304 Pseudotsuga menziesii var. glauca 82 Psylla uncaitoides 220 Psyllidae 294, 301 Pteromalidae 207 Pterophoridae 131 Pulvinaria regalis 225 Pyracantha spp. 221 Pyralidae 131, 296 Pyrrhalta luteola 222 Quercus alba 226 Quercus cerris 244 Quercus ilex 240 Quercus petraea 239, 240, 244, 249 Quercus pubescens 240 Quercus robur 239, 240 Quercus spp. 221, 241 Quercus suber 240 Reeseliella odai 277, 278 Rhinotermitidae 299 Rhizophora 182 Rhodondendron spp. 221, 222 Rhyacionia 246, 296 Rhyacionia buoliana 241, 249, 250 Rhyacionia frustrana 228

SPECIES INDEX

Rhynchaenus fagi 241 Rhyscionia buoliana Schiff. 105 Rhytisma salicinum 165 Rosa spp. 222 Rubus bogotensis 9 Sacchiphantes abietis 256 Salix 157, 164, 182, 190, 197, 205 Salix aurita 154, 156, 157, 158, 164 Salix caprea 154, 156-158, 163-165 Salix caprea x Salix aurita 159 Salix caprea x Salix repens 159 Salix cinera 164 Salix dasyclados 155, 193 Salix eriocephala 155, 164 Salix gracilistyla 198 Salix pentandra 154 Salix phylicifolia 156, 157, 164, 165 Salix purpurea 193 Salix repens 154, 156-159, 163-165 Salix repens Sm. L. 156 Salix sericea 155, 164 Salix spp. 156, 174, 265 Salix tiandra 154 Salix viminalis 10, 154, 155 Sapindaceae 143, 144 Scarabaeidae 302 Scarabidae 298 Schizonatus latus Walker 207 Sciopithis obscurus 222 Scolytidae 132, 299 Scolytus intricatus 241 Scolytus ventralis 35, 49, 58 Semanotus japonicus 277, 278, 279, 280 Septoria 204, 208 Septoria musiva Peck 204 Serjania lethalis 143, 144 Sesiidae 131 Siricidae 131 Solidago altissima 140 Sphaerioidaceae 204 Spodoptera litura 296

331

Stephanotis pyrioides 221 Strepsicrates rothia 297 Strichnos pseudoquina 143 Swietenia 288 Swietenia macrophylla 289, 304 Swietenia macrophylla var. Jacq. 289, 295 Sylvestris 270 Synanthedon scitula 220, 277 Tabebuia ochracaea 143 Taphrorychus bicolor 241 Tectonia grandis 288, 289, 295, 304 Tenthredinidae 131, 156, 242 Terminalia brasiliensis 143, 144 Terminalia ivorensis 288 Terminalia superba 288 Thaumetopoea pinivora 241 Thaumetopoea pityocampa 68 Thaumetopoea pityocampa 68, 240, 241, 244, 247 Thaumetopoea processionea 241 Thecodiplosis japonensis 266, 269. 270 Thecodiplosis japonicus 266 Theobroma cacao 304 Thuja spp. 222, 299 Thyrididae 131 Thyridopteryx ephemeraeformis 221 Thyrinteina arnobia 297 Tilia spp. 222 Tomicus 35 Tomicus minor 49 Tomicus piniperda 38, 44, 49, 52-55, 57, 58, 60-63, 67, 241, 246, 248, 256, 257 Toona ciliata 294 Tortricidae 131, 202, 203, 297 Tortrix viridana 240, 241, 242, 246, 258 Totricidae 277, 296 Totricidae 79 Tsuga 35

332

Ulmus 182 Ulmus americana L. 183 Ulmus spp. 222 Unaspis euonymi 221 Uredinales 204 Vaccimium angustifolium 174 Vaccinium 182 Vatairea macrocarpa 143 Xiphydriidae 131 Xyleborus spp. 299 Xylosandrus 299 Yponomeutidae 132 Zeiraphera canadensis 116 Zeiraphera diniana 245

SPECIES INDEX