IN: Schowal~Er, T.D. and G.M. Filip, , - Eds., Beetle-Pathogen Interactions in Conifer Forests

, IN: Schowal~er, T.D. and G.M. Filip, , - eds., Beetle-Pathogen Interactions in Conifer Forests. Academic Press, London. pp 81-101. 199'. -5-

PETER l. LORIO, JR. USDA Forest Services, Southern Forest Exp. sm., Pinevi//e. LA. USA

5.1 h1troduction 81 S.2 Basisfor UnderstandingSuess EffedS 81 S.3 Host T~ Ontogenyand AtenoloaY 83 S.3.1 Ontogeny 83 5.3.2 PhenoloaY 83 S.4 PhysiologicalOlanges Associatedwith Devel~ent as 5.4.1 Partitioning of Assimilate as 5.4.2 Relevanceto Bark Beetle-Pathogen-Tree Interactions 87 S.S Water Deficits, Trce Developnent and Atysiology 89 5.5.1 Plant FaCtOrsAff~g Responses 89 S.S.2General Pauems of Response 89 5.5.3 Flowering and ReproduCtion 90 S.6 Mechanismsof T~ Defense 90 5.6.1 Theories 90 5.6.2 Oleo~sin inConifm 91 S.7 FactorsAffecting Expressionof Resistance 93 S.7.1 ForeStand StandCooditions 93 S.7.2 CatbOOydrateSwus of Host Trees 94 S.7.3 Enviromnentand Tree Devel~ent 94 S.8 Conclusims 95 RefeJatCes 96

5.1 INTRODUCTION

- " - - -- - Interactions among bark beetles,pathogens, and conifers constinite a triangle. Another ai- angle of interacnons existS among the invading organisms (bark beetles and pathogens), the trees, and the environment How important, variable or constant, simple or complex, is the role of treeSin theseaiangles? Understanding the wide range of interacnons that take place among trees,bark beetles,and pathogens,and betWeenthe organismsand their envi- ronmentS,requires consideration of t1-eeresponSes to flucroanng environmental condinons and the effect of tree responseson tree-invading organisms(Loomis and Adams, 1983). In recent years there has been considerableprogress in researchon interacnonsamong bark beetles,microorganisms, and conifers. This chapterfocuses on a few important ~~ of tree physiology as it affectSnee interacnonswith bait beetlesand pathogens.

5.2 A BASIS FOR UNDERSTANDING STRESS EFFECTS

Biotic and abiotic su-essesof various kinds (Chapter 4) are common during the growth and development of conifer fores~ and vinually all natural systems.Unfonunately. different

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82 P L. LDriD. Jr kinds of stressfrequently are nOtdistinguished, thus hindering our understandingof effects on tree physiological processesand tree interactions with other organisms (Sharpe fotaI., 1985). That deficiency and the general perception that stressis inherently bad for b"eeSand good for invading organisms are major obstacles to better understanding and management of bark beetle-pathogen-conifer interactions. Sb'essdue to water deficit occurs so frequently that, in the long nIn, it reduces plant growth and crop yield more than all other stressescombined (Kramer, 1983). FCI' this rea- son, water supply has been the subject of much study concerning inte~tions among bark beetles,pathogens, and conifers and will be a focus of this chapter. Our limited knowledge of whole-tree physiology, and panicularly stress effects, is imperfectly integrated with the study of bark beetle, pathogen, and conifer interactions. Tree physiology generally has received little attention with regard to solving faestry p-ob- lems (Kramer, 1986). This stare of affairs indicates a need to provide a broad basis UJX>n which to consider the effects of stress on conifers and how Sb'esses,such as water deficits, may affect tree physiology and interactions of trees with other organisms. Kramer (1986) atU'lDutesthe limited use of physiology in forestry to a poor understanding of the role of plant physiology. He specifically focuses on the general lack of apprecia- tion of die concept. developed many years ago, that die nature and limitations of physiological processes are contrOlled genetically, but that the environment determines acblal productivity (Fig. 5.1). Clearly, heredity and environment influence plant growth and development through dleir combined effects on physiological processes.Klebs (1910) pr0- vided some of the earliest input to this concept, and his conbibutions are commonly recog- nized in bom older and recent lirerat\D'e(Krauss and Kraybill, 1918; Loomis, 1932, 1953; Kramer and Kozlowski, 1979; Sachs, 1987). It is interesting and relevant to this chapter that Klebs (1910) worlced with both microorganisms and higher plants.

Fig. 5.1. Diagram illusttat1nS the role of physiology in forestry. Genetic potential and environment must operate through physioloSical processes in determinins the quantity and quality of growth. Expression of resisWlce m«hanisms of conifers to invasion by palhoSen5and bark beetles are lik... wise sova-ned by theserelationships. (From Kramer. 1986.)

ROLE.Of PHYSIOLOGYIN FORESTRY GENET'M:POTENT1AL ENVIRONMENTAL Tree improvement FACTORS programs Atmospheric,soil and biotic Silviculturel tr.~tI

PHYSIOlOGICAL PROCESSES At whole plant level At cell~lar level

QUANmY AND QUAUTY OF GROWTH (Usually fa, below the possible maximum) &vir~lIlaJ SITUS aNi WJJoI..t". PIa:ysiolOlJ 83

5.3 HOST TREE ONTOGENY AND PHENOLOGY

5.3.1 Ontogeny

Tree ontogeny (me devel~ment or course of development of an individual) may be considered in various contexts: a uee's life span from seedling to maturity; the development of cells and their differentiation and maturation; the foonation of specialized tissuesassociat- ed with plant development, and the morphological, physiological, and chemical changes that OCCW'through the seasonsof the year. Physiological changesnormally associatedwith ttee development,apart from severeenvironmental suesses,may have important effectSon ttee susceptibility to and suitability for herbivores and pamogens in general. Fcr example. Coleman (1986) proposes that leaves are most subject to herbivore atta::k at the time of transition from being carrohydrate sinks (recipientS)to sources(synthesizers). Regarding bark beetle, pathogen, and conifer interactions, physiological changes associated with eimer maturation or aging are imponant. For example, when ttees develop a capac- ity to flower and fruit (maturity) an additional demand is pla:ed on photosynthatesp-evi- ously panitioned among vegetative growth and differentiation processes. Given limited energy and material resourceswithin b'eeS.the potential production of oleoresin. a primary factor in resistanceof Pinus speciesto bark beetle attack (Hodges et aI.. 1979), is affected by such developnental changes. Aging eventually leads to slower rates of metabolism, slower wound healing, and reduced resistance to certain insects and fungi (Kozlowski, 1971). Typical hostS for Dendroctonus frontalis have reached matUrity and have grown to large size. Such b'eeS provide abundant food and habitat for colonizing beetles. Their long boles and large diam- eters provide large surface areas to accommodate attacking beetles and brood in numbers greatly exceeding that possible in small uees. All of me various reproductive and vegetative growth and differentiation ]X'OCessesare energy dependent to some degree, and there are multiple inter~tions and competitions among them for available substtates.Carbohydrate relations during growth and development of Pinus sttObili indicate that enlarging cones draw heavily on resources from l-year- old needles early in the seasonand from cun-ent-year needles late in the season(Kramer and Kozlowski, 1979). Thus. it seems mat cones supply little of their own carrohydrare needs for growth and development. mat they can suwress roth apical and cambial growth. and JX}tentially reduce me synthesis of secondary metabolites (defensive chemicals) such as oleoresins. Some understanding of the relationships between reproductive and vegetative growth and development, and how mey may be affected by a variety of environmental conditions over time, is essenbaIto testing effectS of environmental suesses.For example. variation in the timing, intensity, and dmation of water deficitS obviously will affect vegetative and reproductive processesdifferently (Hsiao et al., 1976b).

5.3.2 Phenology

Tree phenology concerns relationships between climate and periodic biological phenomena, such as flowering, bud burst, foliage production, and leaf fall. Stanley (1958) illustrated the general reproductive growth cycle of the genus Pinus (Fig. 5.2), but indicated mat exact time of pollination varies with species, latinlde, site, and elevation. Environmental factors may cause other phenomena to occur earlier or later in a season,as well as shonen or lengthen their duration. Relationships among flowering, cone growth and development, 84 PL.~."

Fig. 5.2. Reproductive cycle of pine. (From Stanley, 1958.) and other seasonalvegetative growth processesare of interest becausecompetition among such processes for available photOsynthateScan affect b'ee resistance to herbivores or pathogens. The U'ansition from earlywood to latewood in Pinus species, the development of the current year's vertical resin doctS, and me seasonalcourse of resin flow are of particular interest in relation to bark beetle attack (Lorio, 1986). During earlywood f(B'Ination,partitioning of carl>ohydrateto oleoresin synthesis is limited by sttOng demands for reproductive and vegetativegrowth processes.As rowsof earlywood~heids areproduced, the target of beetle attack (the xylem/phloem interface) is displaced progressively from the principal oleoresin reservoir (the vertical resin ductS of the preceding and prior years). With me transition to latewood and the development of me current year's venical resin ductS, the potential flow of resin at beetle attack sites in the the cambial regioo increases, as does the infened resistance to beetle attack. Lorio el al. (1990) expla'ed these relationships in testing a concepbJalmodel of seasonalchanges in the resiStanceof P. laeda to D. fronlalis (Figs 5.3 and 5.4). The timing and duration of devel~mental processes,and associated changes in ttee resistance to beetle attack, can be altered considerably during a growing season in response to environmental influerK:es. Envir~lIlQ/ S".cs.raid Whd,.".,. Plt)l.ridOf'1 8'

Fig. 5.3. A concepwaI model of seasonalchanges in pine resis~e to southernpine beetle attack for years which have soil Wa1erbalux:e patterns similar 10 that of the lonl-tenn average. Resislanceto the earliest anackina beetlesis consideredto be highly depaxlent on the potential flow of oleoresin II the wound site. (From Lorio el aI.. 1990.)

5.4 PHYSIOLOGICAL CHANGES ASSOCIATED WITH DEVELOPMENT

Growth response alone may be an unsafe measure of vigor (Kmus and Kraybill. 1918). Tree growth and resistance to bark beetle and fungal invasion are correlated to some degree (Waring. 1983). and resistance may reside in the amount of current and sta'ed photOsynthate available for production of defensive compoWlds (Waring and Piunan. 1985; Christiansen et al.. 1987; Dunn tt al.. 1987). F~tOI'S that greatly influeoce bod1 growth and the production of defensive chemicals include water deficitS and excessive crowdingof ttees. Crowding leads to shOrtenedcrowns. reduced phOtOsynthateSto suppon growth and omer processes. and thereby to reduced synthesis of defensive compounds.Severe water deficitS can reduce cambial growth. but perhaps more importantly they reduce shoot and needle growth. cause ~ablre needle fall. and reduce leaf surface area. with long-lasting effects on photosynthate suWly to suPPOrtgrowth: 'maintenance,aDd production.of defensive chemicals. Apan from effects of crowding, water deficits, and Otherf~tOJ'S, impa'tant physiological changes take place in me cowse of ontogenetic and seasonalgrowth and developmenL

5.4.1 Partitioning of assimilate

SeasonalaspectS of the competition betWeengrowth and the production of defensive chemicals in conifers have not been given much attention. h1 other systems. oowever. me integrative conuol of plant growth and development has been given a great deal of attention (Brouwer. 1983; Chapin el ai.. 1987; Loomis el aI.. 1990). Partitioning of carbon during a growing seasonis panially under genetic coottOl (Fig. 5.1). but p~nology and an may of 86 PL. L«'iD, h

Fig. 5.4. Graphs of water regimes. the course of xylem growth and development. vertical resin duct fonnation. and resin yield in 1984 (.. b. Cod) and 1985 (e. f. g. h). Daily water storage and cumula- tive water deficits (.. e). Tree role cambial growth with total tr~heid counts. time of transition to latewood. and amount of earlywood and latewood fonned (b. £). Vertical resin duct densities in me current year.s growth ring (c. g). OleoJesinyield over 24-hour periods (d. h). Vertical bars are stan- dard errors. n - 10 for 1984. n. 16 for 1985. Results for 1984 approximate the concepblal model shown in Figure 5.3. but those for 1985. a year abnormally dry in spring and early summer relative to long-termaverage conditions. do not. (From Lorio e1aI.. 1990.) EllvirONMnlaJ SITUSGIld Wholc.trcc Physiology 87

~ u C ~ ~ .Q

Fig. 5.5. Carbon partitioning among growdt and developnmtal processesin response to greater or lesser nutrient and water supplies. illustrating the competition betWeengrowth and differentiation processesas well as among systemswithin a tree. (After Goroon and Smith. 1987.) environmental conditions can greatly alter partitioning patterns. especially in the shott term. Substtatesupply is consideredto be a major factor. Supplies of carbon and niuogen assimilates are normally limited. and various sinks com~te for the limited supplies. Gordon and Smith (1987) illustrate how changesin nutrient and water supply may affect activity of apical meristems relative to photosynthesisand an array of growth and developmental processes(Fig. 5.5). If one process removes a sub- sttate from circulation. another cannot use il This competition for limited resourcesresultS in developmental changes(l'rewavas. 1985). Loomis et 01.(1990) refer to this coordination of plant growth and development as a "nutritional theory" of coordination. that is based on the work: of .K1ebs.(1910)~KraUs and.Kraybill (1918). and LOOmi1(1932). Loomis (1932) proposed the concept of growth-differentiation balance as a convenient and simplified schemefor predicting or explaining plant behavicx.

5.4.2 Relevanceto bark beetle-pathogen-tree interactions

Several studies illustrate the great seasonalvariation in physiological responsesto inoculation with fungi vectored by bark beetles (Reid and ShrimptOn, 1971; Paine, 1984; Stephen and Paine, 1985; Cook et al., 1986; Owen et al., 1987; Raffa and Smalley, 1988). Much of the variation may be associated with differences in carbohydrate partitioning due to ontogeny and environment For the study of interactions among bark beetles, fungi, and trees, it is especially imponant to recognize that significant chemical changes OCC1D'sea- 88 PL. LDr'iD,h EnvirOrlmafllalStress ana' Who/c-trcc Ph)I$iolOf'J 89

The ontOgenyand phenology of b'eesare associatedwith physiological changesof great significance to bark beede. pathogen. and b'ee interactions. Further. one should recognize the importance of seasonalchanges apart from environmental suess such as water deficits. as well as me need to evaluate me effectSof water deficits in tenDSof their timing. severity. and duration.

5.5 WATER DEFICITS, TREE DEVELOPMENT AND PHYSIOLOGY

Becauseof itS seemingly overall importance to U"eegrowth and yield (Zahner, 1968), water deficit, rather than the variety of other biotic and abiotic stt'esses(Chapter 4), is the focus of this chapter. Tree responsesto water deficitS, as to other sU'esses,are related to the tree' s stageof development.

5.5.1 Flant factors affecting responses

A plant's response10 water sttess dependson its metabolic activity, morphology, stage of growth. and yield potential (Gardner et al., 1985). Water deficits during vegetative growth phaseshave effects entirely unlike effects during flowering and fruinng, and fruit and seed development and mawranon (Hsiao et al.. 1976b). While cell growth is moSt sensinve to water deficit. xylem conductance reduction may not be affected until water potential is below -0.7 to -3.0 MPa (7 to 30 bars) (Hsiao et a/., 19768; Tyree and Dixon, 1986; Jones. 1989). However. assessingthe effects of water deficits on plants is not a simple problem. Bradford and Hsiao (1982) provided a thorough discussion of inherent difficulnes in understandingthe direct eff~ts of water deficits on physiological processeswithin plants, and on the long-term behavior of plants. They point out that because of feedback loops among various metabolic processes,it is difficult 10 distinguish between cause and effect following the onset of a pernlrbarion. Further, in natme, water stressusually developsgradu- ally, over days to weeks, providing ample rime for coordinated responsesof internal pr0- cesses.and resulting in adaptation and enhancementof survival under sttess.

5.5.2 General patterns of response

Somepatterns of grossplant reSJX>nsesto water stressare generallyapplicable to a large numberof plant species(Bradford and Hsiao, 1982).It appearsthat overall changesin responseto stressalmost always lead to adjusbTlentSin water useand supply that increase the probability of survival and propagationof the species.Bradford and Hsiao (1982) reviewed a number of gross responsesand adaptationsthat occur with many species: reducedfoliage growdt during early water deficit, resulting in reducedtranspiration and a rationing of water supply to meet the demandsof a longer ontOgeneticspan; increases in rootSrelative to shOOtS;osmotic adjustmentthroughout the plant, resulting in maintained tUrgorand physiologicalfunctions 81 reducedwater potential; changesin leaf shapeand orientation,leaf abscission,and closingof stOmates,resulting in reducedlight interceptioo, reducedttanspiration, and conservedwater. Studiesby Linder t't aI. (1987) with Pi~ radiata, and by Cregg et aI. (1988) and Hennesseyet aI. (1992) with P. taeoo,illustrate theseimportant relationships. Bradfordand Hsiao (1982)concluded that insufficientattention has been givtn to plant responsesto water stressthat precedestomatal closure and changesin photosynthesis.In 90 PLLmio.Jr

Pinus. responsesto such deficitS no doubt include greater partitioning of photOSynthatesto oleoresin synthesis, an imIX>rtantresponse relative to resistanceto bark beetle attack (Lorio and Sommers. 1986; Lorio et aI., 1990) .

5.5.3 Flowering and reproduction

The process of flower iniriation in plantS is complex and only panially understood, but Sachs (1987) notes that moisture and osmotic stress and reduced niuogen nutrition can reduce groWth, accelerate flowering, and result in increased carbohydrate concenttarion in shOOtS.In Pinus, which initiate suobili primordia in mid- to late-summer in the southern US, research has demonstrated important relarionships between rainfall and flower initia- rion and cone production (Wenger, 1957; BengtSOn,1969; Shoulders, 1967, 1968, 1973; Dewers and Moehring, 1970; Grano, 1973). Wenger (1957) foamdthat P. taeda seed crops varied directly with May-ro-July rainfall of the second preceding year, and suggestedthat irrigation in seedorchards might be benefi- cial. Early resultSof irrigation Dials with P. elliottii Val. elliottii were ambiguous (BengtSOn, 1969). However, Dewers and Moehring (1970) found that irrigation of P. tae:dain a 13- year-old seed orchard April through June, followed by drought treaunent July through September, resulted in significantly higher conelet production than any other treatmenl Results indicated that a perioo of soil water deficit in P. taeda standsduring or jUSt prior to iniriation of ovulate primordia is condocive to cell differentiation into reprooucrive riss~. Late season irriganon may suppress conelet production. These results suppon Wenger's (1957) fmdings for natural standsofP. taeda, and Shoulder's (1967) findings fa: P. palus- tris and illusttate that nming of water deficit greatly infl~nc:es the nawre of ttee IeSJK>nses. Later studies by Shoulders (1973) with P. elliottii var. elliottii in Louisiana, and Grano (1973) with P. tae:da in southern Arkansas, showed that flowering and seed yields were enhanced by plentiful spring rain followed by moderate water deficits during the summer. These results are consistent with results expected from considerarion of plant growth and differentiation balance principles (Loomis, 1932, 1953), and clearly indicate the need for a broad appro~h to the sn.dy of conifer responsesto Stressessuch as water deficits, and the potential effectS of environmental stresseson carbon partitioning to growth, repnxiucnon. and defensive compouOOs.

5.6 MECHANISMS OF TREE DEFENSE

5.6.1 Theories

Thereis an extensiveliterablre dealing with theoriesof defensivemechanisms and relarionships to energy supply in plants: apparency(Rhoades and Cares, 1976; Feeny, 1976), defensivechemiSb'y (Rhoades, 1979; Schultz and Baldwin, 1982),carbon/nuaient balance (Bryant et al., 1983),resource availability (Coley et aI., 1985;Ba72.az et al., 1987),multiple modes(Mattson et al., 1988; Benyman, 1988),to namea few. Othel' literaturemme specific to bark beetlesincludes Wood (1972), Cates and Alexandel'(1982), Raffa and Berryman (1983), Hodges et al. (1985), MatSOnand Hain (1985), Hain et al. (198S), Sharpeand Wu (198S),Sharpe et al. (198S),Lorio and Hodges(198S) and Lorio (1986). The defensivemechanisms that function in conifers in responseto invasionsby bark beetlesand associatedpathogens seem to centeron someasp«ts of their oleoresinsystems. Envi'OfUMlIlal St,us aNi WAd~-t'c~ PhysidOO 91 In thoseconifers that possessa primary resin system,such as Pinusspecies, the potential rate and durationof flow from woundsis consideredan importantdefensive mechanism (Chapter8). However,induced responses to woundingby bark beetlesor pathogensalso may be importantin Pinus and in other conifers not JX)ssessingprefonned resin systems (Berryman,1972; Chapter 8).

5.6.2 Oleoresin in conifers

Stark (1965) extensively reviewed the subject of oleoresin as a resistance mechanism to attack by forest insects. He considered me subject fundamentally important and of immedi- ate practical applicability. The resin problem has been researched considerably since Stark's review, with much progress. SeeChapter 8 for a discussion of the oleoresin system in Pinus speciesin relation to colonization by baIt beetles. This section focuses on some aspectsof host tree water Statusand the potential for resin to flow from bark wounds. Oleoresin exudation pressure (OEP), measured with glass capillary manometers (Bourdeau and Schopmeyer, 1958), Bourdon gauges(Vi~, 1961), or otha devices such as ~tentiometer-type pressure ttansducers(Helsem and Brown, 1970), generally is perceived to be directly related to resin flow. Howeva, little experimental evideoce is available to suwon this idea. Schopmeyeret al. (1954) reasOnedthat flow through radial resin ducts could be expressed by a modification ofPoiseuille's equation for the flow of liquid through capillaries:

Y = [KN(ab)2P]/r1

where Y is die yield of resin over a fixed time, K is a constant. N is the number of radial resin ductSper unit area of wound surface. (abf is the avuage of squared produCtSof ~ major and minor semiaxes (a and b) of die duct cross section, P is the exudation pressureat die point of discharge. and 11is resin viscosity. Bourdeau and Schopmeyer (1958) found a statistically significant relationship betWeen resin yield per inch of wound width over two 2-week periods of commercially tapped Pinus-elliottii var. elliottii and the functioo

[N(ab)2P1/Il

for variables as defmed above. When P was removed, the relationship was not significanl -They concluded that nurnber and size of resin doc~, pressure,and viscosity were relaled to resin yield from wounds in P. ellioltii var. ellioltii stems and mat pressure, viscosity, and pressure:viscosity ratios might be useful variables in progeny testing because they are under sttong genetic control Since the work of Schopmeyerel ai. (1954) and Bourdeau and Scbopmeyer (1958), few sUldieshave been conducted in which both OEP and resin flow were measuredalong with other variables. In contrast 10the resul~ of Bourdeau and Schopmeyer (1958), Banen and Bengtson (1964) found no correlation between OEP and resin yield from seven seed sources of P. ellioltii var. ellioltU. They did find that me ratio of OEP to viscosity was related to flow, as did Bourdeau and Schopmeyer (1958), but viscosity alone was m

5.7 FACTORS AFFECTING EXPRESSION OF RESISTANCE

As suggestedby Raffa and Berryman (1983), U'eesvary in their quantitative resis~ to invading organisms due to genetic, environmental, and seasonal factOrs. This section focuses on some aspects of the growth and development of U'eesthat could affect the potential expression of defense against bark beetles and pathogens. If the resin systems, primary or secondary,are important to defense, it seemslikely that the partitioning of photosynthates would be very important to the expression of resistance to invasion. Accordingly, U'eeswith large and efficient crowns that produce sufficient photOsynthatesto meet the demands for roth vegetative and reproductive growth, as wen as synthesisof differentiation p-oducts, such as allelochemicals, will likely be more resistant to invasioo than b"eeswith small, inefficient crowns. Several factors, including forest or stand saucture, carrohydrate swus of ttees. and seasonalenvironmental f~tOrs. influence exJX'essionof resistance.The effects of thesefactors may vary with the developmental stage of the ~. 5.7.1Forest and stand conditions

Site quality, speciescomposition, Standdensity, tree ages and sizes, diseaseincidence, and other insect activity are among the many factors that can affect ~ growth and development, and interactions with bark beetles (Waring and Schlesinger, 1985). Growth, especial- l~ .bole Iadial grQwth,often hasbeen viewed as indicative of ttee susceptibilityor resistance to beetle attack (Miller and Keen, 1960; Hicks, 1980; Waring, 1983). Relationships among growth, environment, and invading organisms are complex and confounded, but there is little doubt that crowded stand conditions result in reduced light abstX'ption,leaf area, photosynthesis, growth, and potential production of allelochemicals, compared to uncrowded stands (Waring~ 1983; Christiansen et al., 1987; Lorio. 1980). Funh ennore, merely the close proximity of neighboring trees in such standsgreatly facilitates the move- ment of bark beetles from ttee to ttee (Gara and Coster, 1968). Close spacing may playa more important role in facilitating D. frontalis infestation growth during endemic periods than during epidemics (Johnsonand Coster, 1978). Funher, in standswith closed canopies, beetle aggregation to sources of pheromones may be more effective than in open stands where high insolation and convection disrupt pheromoneplumes (Fares et al., 1980). Thinning often is recommended to reverse the growth reductioo and susceptibility to bark beetle aaack observedat high stand densities (Chapler 11). Few direct teStsof thinning effectS on stand susce~bility to bark beetles have been relX>ned.but Brown et al. (1987) reponed increased resistance of P. taeda to ~k by D. frontalis following thinning of standsto 23 m2ha-l or less. Nebeker et al. (1985) and Wood tt 41. (1985) reviewed thinning 94 P L Lorio, Jr

practices for southern and western Pinus speciesand made recommendationsfor pest management. including consideration of activities that could aggravate pathogen problems. Amman and Schmitz (1988) and Amman et al. (1988) discussedseveral managementstrate- gies, including the use of partial cuts, to minimize losses of P. contorta var. latifolia to D. ponderosae. Several studies conducted in the western US demonstrated that thinning reduced ttee monality to bark beetles (Sartwell and Stevens, 1975; Mitchell et al., 1983; McGregor et al., 1987). As with the southernPinus species,consideration must be given to potential problems resulting from stand distmbance (root diseases,windthrow, dwarf mistle- toe, etC.)(Witcosky et al., 1986). Although the greatest potential benefit would seem to come from well-planned, early, and scheduled thinnings over the life of a stand, thinnings of matlU'e stan~ can result in improved physiological condition of the remaining trees (more phOtOsynthateproouctiOD, leading to more allelochemics proouction). In some instances beetle attack is reduced SO quickly after thinning that drastic changes in the microclimate may be the primary factOr inhibiting beetle activity (Amman et al., 1988; Banos and Amman, 1989)

5.7.2 Carbohydrate status of host trees

The carbohydrate status of hoSt trees determines nee ability to produce or mobilize compounds critical for defense against bark beetle a~k (Christiansen el aI., 1987) (X defense againSt infections by pathogenic fungi (Shigo, 1985). The littJe-explored literature on d1e formation of lightwood (oleoresin-saturated woody tissue) seems panicu1arly relevant to this issue (Schwarz, 1983; Swbbs et al., 1984; Chapter 8). Pinus responsesto paraquat, a bipyridilium herbicide, applied in awropriate concentra- tions to living stem tissue beneath the outer bark, results in extensive resin soaking of d1e xylem. Years of intensive research on this process in Pinus species demonsttated clearly that the CUJTentand stOredphOtosynthate staWS of uees at the time of tteaanent is imlX>r- tant to the responseobtained (Brown el al., 1976, 1979; Wolter and Zinkel, 1984). In general, spring applications (when carbohydrate stablSnormally would be high) prodtx:es the best average oleoresin yields (Stubbs et al., 1984). Physiological responses to paraquat application include ethylene syndlesis and heightened respiration, both of which are associ- .ated_with~«U~woundingresponse and sttess (Wolter and Zinkel, 1984). Fungal colonization of phloem and xylem in association with bark beetle a~ks appear to elicit similar responses(Berryman, 1972; Raffa and Smalley, 1988; Chapter 8). The namre and extent of response. . probably is. mediated by the same factors that influence response to paraquat applicauons. 5.7.3 Environment and tree development

Drought may play an impa'tant role in the devel~ment of insect outlxeaks (White, 1974; Manson and Haack, 1987; Chapter 4). Martinat (1987), however, questioos the role of "climatic release" as a mechanism to explain widespread periodic outbreaks, l8I'tia11y~~~~ of methooologicaJJB'Qblems. FlD1her, Coonrx (1988) and McQuate and Connor (199Oa,b) TeJX)nresultS of sttldies with Corythucha arcuata on Quercus alba, and Epilachna \lari\l~stis on Glycine max dlat are inconsistent with, and contrary to, White's (1974) hypothesis thai water deficit leads to improved insect performance and abundance.Re(:ently, Tmchin ~t al. (1991) concluded that outbreaksof Dendroctonusfronzalis are not driven by stochasticfloc- ttlabonsof weather,but by someunknown ~u1aIion process~g in a delayeddensity- EnvVOllm6l1lalSuus Gild Whol~.,,~~PhysiolOf1 9~ dependent manner. While severe water deficitS may greatly reduce nee resistanceto bark beetle attack (Vire, 1961; Lorio and Hodges, 1968a, 1977), it does not follow that bark beetle outbreaks will necessarilyoccur. Further, it is important to realize that general relationships vary among speciesof insectS,pathogens, and D"ees. In the south and southeast.severe droughtS usually ale associatedwith high temperatures during the mid- to late-summer, conditions that are typically unfavorable for adult beetle survival and brood development (Gagne el aI., 1980). Moreover, drought seldom, if ever, developsso rapidly that plantSdo not havean oppon\D1ityto leSJX>ndphysiologically in a manner that will enhancetheir survival and reproduction. A developing drought should limit growth before it limitS photOsynthesis,resulnng in more caroohydrate for processesoth~ than growth. However, carbohydrate use for respiranon may increase temporarily (Brix, 1962). Perhaps,if drought severely depletes carbohydnte levels by reducing effective leaf area, the responseof photOsynthesisto improved water conditions may be lower than neces- sary to meet needsfor growth and developmentas drought is alleviated Inoculation studies with pathogens or fungal associatesof bark beetles could benefit from consideration of envi."'Onmentaland developmental factors that can affect results. For example, Chou (1982), working with P. radiala and Diplodia pinea, a fungus that causes shoot dieback, found d18tsusceptibility flucroates with season,being high in spring-summer but low in auwmn-winter. He concluded that seasonalpredispositioo is important in planning inoculation Dials for any P'D'POse.Swdies with a variety of organisms and b'ee species suppon Chou's conclusion. Paine (1984) found significantly different rates and lengths of lesions formed in response to inoculation of the mycangial fungi of DendrOClonusbrevicomis in P. ponderosa from spring through aummn. Owen el al. (1987) found P. ponderosa seedlings to be more susce tibl a number of fungi isolated from Dendroclonus spp. UI'1ngs oot e onganon than 'o...f+e.r b vcl S'~t" Myers (1986), working with several Pinus speciesand Bursaphelenchusxylophilus. found greater mortality from spring inoculations..when cambial octivity was greater, than from late summer and autumn inoculations.

5.8 CONCLUSIONS

The greatestchallenge in the study of interactions among bark beedes, pathogens, and host conifers is to integrate the roles of all three elementSeffectively. The physiology of host fIees has been the least effectively integrated element in past research, ~al1y becauseof a generally pcx>runderstanding of the role of plant physiology in fthcsesin expianauxy. rather man Slabstical. mooe~ an approachsfIOngly enoorsedby Loomis and Adams (1983). 96 PL. L

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