sign in sign up
<<
Home , Betula lenta, Betula populifolia, Ilex opaca, Liriodendron, Platanus occidentalis, Populus grandidentata

Mortality Following Defoliation by the European Gypsy (Lymantriadispar L.).in the. : A Rev,ew

Christopher B. Davidson, Kurt W. Gottschalk, and James E. Johnson

ABSTRACT. This review presents information related to defoliation by the European gypsy moth (Lymantria dispar L.) and subsequent tree mortality in the eastern United States. The literature describingdefoliation-induced tree mortalityis extensive,yet questionsstill remain concerning(1) the associationbetween initial stand compositionand subsequenttree mortality,(2) the influenceof site qualityon tree mortality,and (3) observeddifferences between mortalityrates in initial and subsequent outbreaks. Our review and analysis of the available literature indicates that initial composition affects subsequent defoliation. Stands with predominantlysusceptible host species have higher levels of species-specificand total mortalitythan mixed stands of susceptible, resistant, and immune host species. Differencesin mortalityon sites of varyingproductivity do not appearto be a direct result of site quality; rather, site quality indirectlyinfluences mortality rates through its effect on species composition and therefore defoliation. Differences between initial and subsequent outbreaks appear to be due primarilyto losses of vulnerableoaks and lowercanopy species duringthe initial outbreak; oak mortality in initial outbreaks was found to be significantlygreater (P = 0.0727) than oak mortality in subsequent outbreaks. FOR.Sc•. 45(1):74-84.

Additional Key Words: Defoliationeffects, vulnerability,stand dynamics, ,Lymantriidae.

mosteasily observed effect, and thusthe onethat garnersthe (Lymantriadispar L.) (Lepidoptera:Lymantriidae) majorityof publicand scientificattention. hasORMORE beenTHAN responsible ACENTURY, for thedefoliationEuropean outbreaksgypsymothof Defoliators are endemic within forest ecosystems; however, varyingseverity in easternand north-central forests of North the gypsymoth is uniquebecause of its exoticpest status, America. From its first introductionin 1869 to the early polyphagoushabit, and the increasedpotential for extensive 1960s,defoliation episodes were concentrated in the north- defoliationwhen comparedto native defoliators(Crow and ern hardwoodand oak forestsof New Englandand the Mid- Hicks 1990, Liebholdet al. 1994). The gypsymoth is an Atlantic states.However, population expansion has contin- outbreakspecies. Population densities are cyclicaland are uedto bringthe insectinto contact with standtypes that have characterizedbyextended periods of lowdensity, sudden, rapid neverbeen subjected to a gypsymoth outbreak.Like other increasesto high densitieswhich can be sustainedover an defoliators,the primaryeffects of gypsymoth feedingon extendedperiod, followed by subsequentpopulation crashes treesare reductionsin tree growth,flowering, and fruiting, (Montgomeryand Wallnet 1988). Duringthese periods of andindividual tree mortality. Though all reducethe monetary populationexpansion, extensive areas of forestedland may andaesthetic value of treesand forests, tree mortality is the experiencedefoliation and associated tree mortality.

ChristopherB. Davidsonis Research and DevelopmentManager with Champion International, Eastern Carolina Region, P.O. Box 309, Roanoke Rapids,NC 27870•Phone: (252) 533-5013; Fax:(252) 533-5060; [email protected]. Kurt W. Gottschalkis a ResearchForester w•th the USDA Forest Service, Northeastern Forest ExperimentStation, 180 Canfield Street, Morgantown,WV 26505. James E. Johnsonis Extension ProjectLeader-Natural Resources and Professorwith the Departmentof Forests/,College of Forests/andWildlife Resources, 228 CheathamHall, VirginiaTech, Blacksburg,VA 24061. Acknowledgments:This researchwas supportedby funds providedby the USDAForest Service, NortheastemForest ExperimentStation.

Manuscript received May 22, 1997. AcceptedJuly 10, 1998. Copyright¸ 1999 by the Society of American Foresters

74 ForestSctence 45(1) 1999 While manyspecies of treesand shrubsare utilizedas more susceptibleto defoliationthan standscontaining a foodsource, gypsy moth larvae exhibit a decidedprefer- mixtures of susceptible,resistant and immune species encefor certainspecies. Consequently, researchers have (Bess et al. 1947, Gottschalkand Twery 1989, Houston historically categorizedforest accordingto their and Valentine 1977). Once defoliated, these stands are relativesusceptibility to defoliation(Mosher 1915). These alsomore likely to suffersome form of damage,most often attemptsat categorizationwere essentiallyfor the sakeof tree mortality(Campbell and Sloan1977). Standvulner- convenience.In reality, larval feeding preferenceis a ability,the probability of damagefollowing defoliation, is continuum,dependent on variousexternal factors such as thusgreater in standsof susceptiblespecies. A generalized populationsize andthe availabilityof food. One of the theoryregarding the influenceof speciescomposition on most recent classificationsystems separates trees and subsequentmortality in gypsymoth defoliated stands first shrubsinto three groups,those described as either "sus- emergedduring the late 19th and early 20th century ceptible," "resistant,"or "immune" to defoliation (Mont- (Forbush and Fernaid 1896, Mosher 1915, Clement and gomery1991, Twery 1991, Liebholdet al. 1995). Suscep- Munro 1917). Though no formal experimentshad been tible tree speciesare describedas thosewhich are con- conducted,it was widely believedthat standscontaining sumedby all larval stages,while resistantspecies are large numbersof speciesunfavorable for gypsy moth consumedby only somelarval stagesor whensusceptible consumption(i.e., resistantand immunespecies), would speciesare not available; immune species are rarely if ever not sufferdefoliation and mortality. These ideas were the consumedby any larval stage(Table 1). Their inherent basisfor researchregarding possible silvicultural control susceptibilityor resistancealso results in speciesexhibit- of the gypsymoth through the removal of favoredspecies ing differentialgrowth and mortalityresponses subse- from susceptiblestands (Clement and Munro 1917, Baker quent to defoliation. and Cline 1936, Korstian and Ruggles 1941). Both past This notionof susceptibilityis also applicableat the and presentsilvicultural control methodstheorize that a standlevel, wherestand susceptibility refers to the likeli- reductionin the percentagecomposition of susceptible hood that defoliationwill occur if the gypsy moth is specieslowers stand susceptibility(Gottschalk 1993). present(Bess et al. 1947). Previous researchindicates that Whetherreductions in the numberof susceptiblespecies purestands of susceptiblefood species, such as oaks, are also lowers standvulnerability remainsto be seen. Table 1. Examples of some trees and common to the Eastern United States, and their classificationaccording to currently eccepted gypsy moth host preferenceclasses; adapted from Montgomery 1991, Twery 1991, and Liebhold et al. 1995.

Feedingpreference class Crown position Susceptible Resistant Immune Overstory Betula nigra Acer negundo Abies balsamea Abiesfraseri Betula populifolia Acer saccharum Acer saccharinurn Larix decidua Betula lenta Aesculus glabra Larix laricina Carya spp. Aesculus octandra Aesculushippocastanum balsamifera Populus grandidentata Picea spp. Catalpa speciosa Populustremuloides Pinus spp. Celtis spp. Pyrus malus serotina Fraxinus spp. Quercus spp. Prunus avium Gleditsia triacanthos Salix spp. Populusdeltoides Gymnocladusdioicus americana Sassafrasalbidum Ilex opaca Juniperus virginiana Tsuga caroliniana acuminata Morus rubra occidentalis Robinia pseudoacacia Ulmus rubra

Understory Carpinus caroliniana Amelanchier arborea Acer pensylvanicum Corylus americana Cornus Acer spicatum Crataegus spp. Oxydendrumarboreum Cercis canadensis Hamamelis virginiana Prunus pensylvanica Diospyros virginiana Ostrya virginiana Prunus virginiana Kalmia latifolia Vaccinium spp. Rubus spp. Viburnum spp.

ForestSctence 45(1) 1999 75 Thoughspecies composition often takes center stage in prudentto review the relevantfactors in detail before a discussionsof foreststand susceptibility and vulnerability, discussionof theeffects of gypsymoth defoliation. Whether descriptionsof susceptibleand resistantforest types fre- a treesuccumbs to mortality,or merelyexperiences a short- quentlyinvolve references to specificsite factors.Suscep- term reductionin growthincrement following defoliat•on tible forestshave been described as thoseoccurring on dry dependson the followingfactors: the treespecies; the inten- ridgesand sandy plains, where stands are composedmainly sity,duration, and frequency of defoliation;the tree's physi- of slow-growing,susceptible species and frequentlyhave ologicalcondition at the time of defoliation;and the presence hada historyof bothnatural and anthropogenic disturbance of secondary-actionorganisms such as spp.and (Besset al. 1947,Houston and Valentine 1985). Conversely, Agrilusbilineatus (Weber) (Wargo and Houston 1974, Dunbar Houstonand Valentine (1985) describedresistant stands as and Stephens1975, Houston1981, Parker 1981, Wargo thosefound on mesic ridges, slopes, and bottomlands, where 1981a).These factors do not act independently;rather, •t is standswere primarily mixtures of susceptibleand resistant their action in combination that determines the final outcome. speciesand moisture was not a limiting factor.These classi- For instance,while healthyoaks are able to recoverfrom fications,however, refer only to thelikelihood of defoliation; successivedefoliations during periods when they are not thequestion is whetherthese susceptible sites are also more experiencingother significantstress, defoliation during or vulnerable. References to observed differences in rates of followinga severedrought has been shown to increasethe mortalityon differentsites have been made by a numberof probabilityof mortality (Baker 1941, Campbelland Sloan scientists(Bess et al. 1947,Campbell and Sloan 1977, Hous- 1977). In observationsof oak declinefollowing defoliat•on ton 1981, Gottschalkand Twery 1989). Whetherthis is due by theoak roller(Croesia [Argyrotoxa] semipurpurana to site conditionsdirectly influencing the vulnerabilityof Kearfi) in ,$taley (1965) noted that while individualtrees or whole stands, or issimply a functionof site defoliationwas the primary causeof decline, severityof conditionsaffecting species composition, and thus defolia- declinedepended on bothclimatic and edaphic factors. tion and mortality, is unknown.If thesedifferences can be Defoliationintensity is a measureof theamount of foliage quantified,the identificationand classification of both sus- that is lost duringa defoliationepisode; it is typicallyex- ceptibleand vulnerable stands by sitewould become feasible. pressedas the percentageof foliage removedduring the As gypsymoth populationshave expandedfrom their growingseason. Past descriptionsof defoliationintensity zone of original introduction,differences in rates of tree have frequentlyplaced trees into one of threeclasses; those mortalityhave beenobserved between areas experiencing experiencingless than 30% defoliation(light), 30 to 60% initial outbreaksas a result of new introductions,and those defoliation (moderate), or greater than 60% (heavy) experiencingsubsequent outbreaks from established popula- (Gottschalk 1993). Light defoliationgenerally resultsm tions.This may be a resultof reduceddefoliation in thelatter, minimalvisual or physiologicaldamage, while moderate and dueto theloss of susceptiblespecies; or it maybe theresult heavydefoliation may cause heavy damage. The durationof of geneticselection favoring oaks that are better able to defoliation refers to the number of consecutive defoliation survivedefoliation (Kegg 1971, Campbell and Sloan 1977). episodesthat occur in a giventime period, while frequency of Confirmationof a differencemay shedsome light on these defoliation refers to the number of defoliation outbreaks that hypotheses;it would also affect decisionsmade by forest occurin a giventime period(i.e., how far apartthe outbreaks managersconcerning control efforts for the gypsy moth are, every4 to 5 yr or every 10 to 12 yr). As the numberof under these different conditions. consecutiveepisodes increases, the probabilityof treemor- The previousobservations accentuate the importanceof tality rises(Campbell and Sloan 1977). Heavy defoliation threetopics of interestto bothforesters and entomologists. Is frequentlyoccurs as a singleevent duringa gypsymoth therean associationbetween initial standcomposition and defoliation outbreak;however, 2 or even 3 yr of heavy subsequentmortality rates of treesdefoliated by the gypsy defoliationhave been recorded(Kegg 1973, Tigner 1992, moth? Does site quality influencethe mortality rate? Do Davidson1997). Following a singleheavy defoliation in oak- initial outbreaksin previouslyuninfested areas inflict more hickoryforests in ,Tigner (1992) reported 23% oak damagethan subsequent outbreaks? Though they have been mortality;two defoliationepisodes increased this figureto the subjectof frequentdiscussion, these specific questions 30%, and after three defoliationepisodes, oak mortality havenot been thoroughly examined through the use of either averaged50%. designedexperiments, or througha critical review of the Susceptiblehardwoods, such as oaks, are often com- literature.Therefore, our objectiveis to providea critical pletelydefoliated during an outbreak,but if notphysiologi- synthesisof the availableliterature in orderto elucidatethe cally stressedthey are able to recover. Instancesof trees relationshipbetween gypsy moth defoliation and subsequent undergoingconsecutive complete defoliations followed by treemortality in theforests of the easternUnited States. recovery are not uncommon(Kulman 1971). As a rule, following heavy defoliation,conifers are more vulnerable Factors Influencing Tree Mortality thanhardwoods (Schowalter et al. 1986). Baker(1941) found Following Defoliation thatwhen eastern white pine (Pinusstrobus L.) defoliauon exceeded80%, treemortality was nearly three times greater The etiologyof individualtree mortalitysubsequent to than that of trees defoliated less than 80%. Possible mecha- insect defoliationis extremelycomplex. Therefore, it is nismsfor the differingresponses to defoliationobserved in

76 ForestSctence 45(1) 1999 hardwoodsand conifers have focused on patternsof carbon havedescribed the speciesresponsible for oak mortalityas storageand foliage loss and replacement. While Armillaria mellea (Vahl, Quel.), but recent taxonomicad- speciestend to storethe majorityof their carbonin woody vanceshave indicatedthat this assumptionis incorrect tissues,evergreen conifers also utilize their needlesfor car- (Watlinget al. 1991).Studies in southwesternPennsylvania bonstorage (Kulman 1971, Krause and Raffa 1996).There- have revealedthat the speciesmost commonly affecting foredefoliation of evergreenconifers results in a greaterloss mixedoak stands in thisregion is Armilla ria bulbosaBarla-- of storedenergy and a higherprobability of mortalityfollow- synonymsA. gallicaMarxm. andA. lutea Gillet (Twery et al. lng defoliation (Kulman 1971, Krause and Raffa 1996, 1990).Similar relationships were observed in anextensive Schowalteret al. 1986). In addition,unlike deciduous hard- study of forest sites throughoutthe state of ,conifers are not adapted to rapid leaf turnover and this (Blodgettand Worrall 1992).Of 34 treespecies examined, may contributeto their inability to withstandcomplete or hardwoodswere predominantly infected with A. gallica,A. consecutivedefoliation episodes (Schowalter et al. 1986). geminaB6rub6 & Dessureault,and A. calvescensB6rub6 & The greatestsingle indicator of thelikelihood of mortality Dessureault;when oaks were separatedfrom other hard- •sphysiological condition at the time of defoliation.Research woods,A. gallicaoccurred on approximately 90% of infected hasconsistently shown that treesin poorcondition suffer trees(Blodgett and Worrall 1992). greatermortality; for example,suppressed and intermediate In additionto Armillaria,mortality following defoliation trees are frequentlykilled following a single defoliation has been attributedto subsequentinfestation by Agrilus (Campbelland Valentine 1972, Campbell and Sloan 1977). bilineatus(Weber), the twolinedchestnut borer (Dunbar and Starchis an abundant reserve carbohydrate in and is an Stephens1975, Dunn et al. 1986).Both Nichols (1968) and importantmeasure of physiologicalcondition (Parker 1981, Dunbarand Stephens(1975) reportedthe presenceof A. Kozlowskiet al. 1991).Artificial defoliation of youngblack bilineatusin a significantpercentage of deador dyingoaks oak (Quercusvelutina Lamarck), white oak (Q. alba L.), and followingdefoliation. As with Armillaria, the level of dor- sugarmaple (Acer saccharurnMarsh) by Wargo (1981b), mant seasoncarbohydrate storage has been linked to A. revealeda significantreduction in starch content. Reduc- bilineatus infestation(Dunn et al. 1987, Dunn et al. 1990). tions in root starch levels have also been associated with Dunn et al. (1987) found that white oaks containinglow increasesin glucoseand fructose (Parker and Houston 1971, levelsof storedcarbohydrates during the dormant season had Wargo1972). Some authors have suggested that these changes greaterincidence of borerattack. In addition,though borer areinitiated by defoliationand reflect a conversionof starch attackwas alsoobserved in treeswith higherstarch levels, to sugar(Parker and Houston 1971, Wargo 1972,Wargo and only thosewith low root starchlevels sufferedmortality. Harrington1991). This creates conditions that are beneficial While we havediscussed the impactsof Armillaria andA. to thegrowth of a numberof fungalspecies, thus defoliation bilineatusseparately, in manyinstances both organisms are may indirectly encourageincreased fungal invasion and involved,and the relativeimportance of one over the other subsequenttree mortality (Parker 1981, Wargo 1981a). cannotbe distinguished(Wargo 1977). Thefungal organism most frequently cited in referencesto Fromthe preceding discussion it is obvious that tree death defoliation-inducedmortality is Arrnillaria spp.,a root rot cannotbe attributedto defoliationalone. The probabilityof fungus.Armillaria spp. are ubiquitous in foreststhroughout mortalitydepends on a complexinteraction of manydifferent , and under normal conditions, root infection factors,biotic and abiotic. This inherent variability makes the •slimited by thehost tree (Kile et al. 1991).When stressed by explanationof defoliation/mortalityrelationships and the external factors such as defoliation, however, resistanceto accurateprediction of mortalityextremely difficult. refectionis lowered,and the possibilityof colonizationby Armillaria increases(Wargo and Harrington 1991). Parker Relationships Between Defoliation and andHouston (1971) describedan apparentrelationship be- Tree Mortality tweensugar defoliation and subsequent infection by Arrnillaria. They notedthat while timing and intensityof In the easternUnited States, the dynamicsof gypsymoth defoliationinfluenced dieback of individualbuds and twigs, defoliationand tree mortalityhave beenstudied in different treemortality appeared to be dueprimarily to fungalinva- forestcommunities, at differenttimes and with wide variations sion.Based on examinations of stemsand cut stumps, Dunbar in gypsymoth population levels throughout the years.As a andStephens (1975) concluded that Armillaria played only result,a numberof consistentrelationships have been observed: a minorrole in oak mortalityin .However, the (1) susceptibletree species are defoliated at higherrates and resultsof a studyby Wargo(1977) provideevidence that frequentlysuffer greater mortality than resistant species; (2) tree Armillariacontributes significantly to oakmortality follow- mortalityincreases as the intensity, duration, and frequency of mggypsy moth defoliation. Examination of theroots and root defoliationincreases; (3) treesin thelower canopy (those in the collarsof living, dying and deadtrees showed Armillaria suppressedand intermediate crown classes) have a higher prob- presentin 42% of livingtrees and 96% of deador dyingtrees abilityof beingdefoliated and dying, than trees in the upper (Wargo 1977).In addition,recent studies in Michiganhave canopy(dominants and codominants); (4) physiologicalcondi- revealedthat Armillaria playsa key role in the mortalityof tion priorto defoliationdirectly influences the probability of quakingaspen (Populus trernuloides Michx.) following gypsy mortalityof individualtrees--those in goodcondition are less moth defoliation(Hart 1990). Historically,many authors likelyto diethan those in poorcondition.

ForestSctence 45(1) 1999 77 Studiesin New Englandutilizing the Melrose High- Table 3. Crown conditionand 5 yr stem mortality rates following a single severe defoliation and two consecutive heavy defolia- lands data [see Campbell and Valentine (1972) and tions in a compositemixed stand of matureoaks (Quercus rubra, Campbelland Sloan (1977) for descriptionsof theoriginal Q. velutina,Q, coccinea, Q. alba) in easternNew England.1 From MelroseHighlands data set] provided a first glimpseat the Campbelland Sloan (1977). relationshipsbetween tree species,gypsy moth defolia- Stemmortality (%) tion, and tree mortality. Minott and Guild (1925) and Crown Baseline One Two Baker (1941) bothobserved that susceptiblespecies were condition mortality2 defoliation defoliations defoliated at a much higher rate than resistantspecies. Good I 7 22 These differential defoliation rates resulted in increased Fair 3 19 50 mortality among the susceptiblespecies (Baker 1941). Poor 9 36 55 Further analysisof the Melrose Highlands data verified 1 The composite mixed oak stand consisted of data that was summarized these early observationsand also confirmed the impor- from 122 plots that were measured between 1911 and 1921. tance of crown class, physiologicalcondition prior to 2 Trees used for the baseline mortality estimate had not been severely defoliated for at least 5 yr, and rates were calculatedat the end of an defoliation, and the duration of defoliation episodes additional 5 ¾r period. (Campbelland Sloan 1977, Campbell 1979). Mortality rates were highestamong trees in the suppressedcrown hasbeen observed in field situations.In addition,intraspe- classand lowest amongdominant trees (Table 2). Trees cific variation is often such that individual trees of the same describedas being in goodcondition prior to heavy defo- speciesmay experience significantly higher rates of defoha- liation had lower mortality rates than thoseclassified in tionthan their neighbors (Minott and Guild 1925,Campbell poor condition, and tree mortality increased with the and Sloan 1977, Gansneret al. 1993). Nevertheless,it is well duration of defoliation (Tables 2 and 3). documentedthat forest stands containing large proportions of These relationshipsalso have been observedin other susceptiblespecies suffer extensive defoliation in the event regions and forest cover types subjectedto gypsy moth of a gypsy moth outbreak.But what part does the initial defoliation. Crown class and crown condition were found to speciescomposition play in the resultantmortality that is play a majorrole in defoliation-inducedmortality in studies observed? of forestsin Pennsylvania,,and RhodeIsland. Based on subjectiveobservations, some authorshave Followingtwo outbreaksin thePocono Mountains of Penn- concludedthat stands containing a highproportion of resis- sylvania, much of the observedtree mortality occurredin tantspecies would also be lessvulnerable to mortality(Kegg overstockedstands, and smaller, lower quality oaks suffered 1971,Campbell and Sloan 1977, Stephens 1988). There are thehighest mortality rates (Gansner et al. 1983,Gansner et al. severalstudies in whichthe authors have enumerated species 1993).In mixedstands in RhodeIsland, more than 90% of all differences,and these appear to confirmthis theory. The best deadstems and 63% of thetotal basal area lost subsequent to exampleof differentialdefoliation and mortality due to defoliationwere in the suppressedand intermediatecrown speciescomposition is given by Brown et al. (1979), who classes(Brown et al. 1979). In oakdominated forests in New studiedmixed oak, oak-pine, and mixed hardwood stands in Jersey,Stalter and Serrao(1983) foundthat large, old trees Rhode Island. The stands were defoliated four times; two and smallsuppressed trees died at the highestrates, results heavydefoliations (60-90%) in 1971and 1972,followed by that were similar to thoseobserved by Kegg (1971). The 2 yr of defoliationbelow 60%. A significantreduction in durationof defoliationepisodes influenced tree mortality in overalltree mortalitywas observedas the proportionof oak botha northernhardwood forest in New Jerseyand southern declinedwithin a standand the numberof resistantspecies Appalachianhardwood forests in Virginia(Kegg 1971, Tigner increased(Table 4). Standswhose original basal area con- 1992).During the course of an outbreakin New Jersey,oak tainedapproximately 98% oak experiencedmortality rates mortality increasedwith eachsuccessive defoliation, from that were morethan threetimes greater than stands which 6% to 69%, overa 4 yr period(Kegg 1971). originally containedonly 29% oak. Brown et al. (1988) Initial StandComposition observed similar trends in mixed stands in Rhode Island in the Althoughwe continueto classifyforest trees as either early 1980s.Stands containing a largepercentage of oakshad susceptibleor resistantto defoliation,considerable variation morethan double the mortalityof thosewith a largepercent- age of easternwhite pine (Table 4). The primaryresistant speciesin bothcases were conifers; however, this pattern of Table 2. Five-yearstem mortality rates, following a single heavy defoliation, of dominant and intermediate/suppressed trees in a a reductionin mortalityfollowing a reductionin the propor- compositemixed stand of mature oek s ( Quercusrubra, Q. velutina, tionof susceptiblespecies was also observed in bothnorthern Q. coccinea,Q. alba)in easternNew England.1 FromCampbell hardwoodand southwesternPennsylvania mixed hardwood and Sloan (1977). standswhere the resistantspecies encountered were other S•m mortality(%) hardwoods(Campbell and Sloan 1977, Fosbroke and Hicks Crowncondition Dominant Intermedia•upp•ssed 1989).Campbell and Sloan's (1977) analysisof theMelrose Good 3 12 Highlandsdata between 1911 and 1921clearly showed that Poor 22 41 reductionsin the proportionof susceptibleoaks within a

1 The composite mixed oak stand consistedof data that was summarized standreduced total mortality (Figure la). Fosbrokeand Hicks from 122 plots that were measured between 1911 and 1921. (1989) foundthat stands with lessthan 60% of theirbasal area

78 ForestSctence 45(1) 1999 Tabla 4. Total mortality as a percentaga of initial stand basal area, and oak mortality as a percentaga of initial oak basal araa, observed in Rhode Island forest stands with varying proportions of oak basal araa prior to defoliation. Mortality(%) Standtype Oak BA (%) Oak Total Reference Mixed oak 98 i 8 i 7 Brown et al. 19791 Oak-pine 60 9 7 Mixed hardwood 29 5 5

Oak-pine 60 6 i 7 Brown et al. 1988: Pine-oak 39 4 9 Pine 3 -- 7

1 Number of study plots was not given; study period was 1971 to 1975. 2 n = 18 plots;study period was 1981to 1983. in oakshad lossesthat were comparableto undefoliated with varyingproportions of oakand found a similarrelation- stands,while those with more than 60% exhibited a distinct ship; the greaterthe percentageof oak, the greaterthe increasein mortality(Figure lb). defoliationpotential. These differential defoliation rates con- It is clearthat total mortality following gypsy moth defo- tributedto the observed differential mortality exhibited within liatlonwill riseas the percentage ofoakbasal area in thestand thesestands. Brown et al. (1979) alsofound that in addition increases(Campbell and Sloan 1977, Brown et al. 1979, to differencesin total mortality,species specific mortality Fosbrokeand Hicks 1989). This indicatesthat there is an ratesalso varied. Oak mortalitywas observed to increaseas underlyingrelationship, and we canidentify two plausible the total amountof oak increasedwithin the stand(Table 4). explanations(Figure 2). In thefirst case, increased mortality Thesedifferences in speciesspecific mortality rates were may be attributedto changingproportions of susceptible alsoobserved by Brownet al. (1988),albeit on a smallerscale species(i.e., the food base)affecting the dynamicsof the (Table4). Brownet al. (1988)also noted that the mortality of larvalpopulation within the stand (Figure 2b). As thepropor- resistantwhite pine was greatestin standswith a large tion of susceptiblespecies within a standincreases there is a percentageof oaks,where the pine occurred as an understory concomitantincrease in the intensity,duration, and fre- species.Increasing mortality of resistantspecies as a resultof quencyof defoliation.This in turnresults in elevatedspecies specificmortality rates and greater total mortality than would be expectedbased on the differencein composition.In the secondcase, species specific mortality rates are assumedto Purestand comeosition va. Mixedstand comDosition 30sq. m/ha of susceptible species 15sq. mlha of susceptible species be independentof composition,and the observed increase in 15 sq. m/haof resislantspecies mortalityis simplya functionof theproportion of susceptible speciespresent as expected by thedifference in composition, 1 e, defoliationof a large numberof susceptiblespecies resultsin a largeamount of mortality(Figure 2c). Are either of these explanationscorrect? Results from a number of studiessuggest that the observeddifferences are dueto the lossof 24 sq. m/ha = 80% mortality Va. lossof 4.5 sq. m/ha = 30% mortality former ratherthan the latter. Brown et al. (1979) foundthat rateof suscepliblespecies, or tale of susceptiblespecies, or 80% mortalityrate of all species 15% mortalityrata of all species standscomprised of 98% oak experiencedsignificantly greaterdefoliation than stands with only 29% oak. Campbell andSloan (1977) computeddefoliation potentials for stands e) b) 50- 50-

lossof 15 sq.m/ha = 50%mortality va. Jossof 7.5 sq.mlha = 50%mortality tale of susceptiblespecies, or tale of susceptiblespecies, or 50% mortalityrate of all species 25% mortalityrate of all species Figure 2. Diagram depicting the possible relationships between stand composition,defoliation, and mortality rates, showing (a) the original stand composition of hypothatical pure and mixed stands pdor to defoliation; (b) due to a graatar proportion of suscaptible species in the pure stand, dafoliation intensity, duration and frequency increasa, rasulting in elevated specias •k • • (%) Oakb•l a• (%) specific mortality rata and total mortality graater than that expectedbased on diffarencein composition;i.e., total mortality Figure 1. Infiuance ef initial oak basal area on tree mo•al• (pure stand) = 2 x total mortality (mixad stand);(c) following subs•uent to gypsy moth dafoliation in (a) mix• oak •ands in dafoliation, overall species specific mortality ratas am the same New England,data was obtaln• from 122 plots (Campbell and in both stands, but due to a larger total initial basal area of Sloan 1977); and (b) mixed ha•ood •ands in sethwestern susceptible species, tha pura stand has a greater amount of total Pennsylvania,data was o•ain• from 237 plots (Fosbrokeand mortality; an expected result based on the diffarance in Hicks 1989). composition.

ForestSctence 45(1) 1999 79 an associationwith largenumbers of susceptiblespecies has siteindex to separatedifferent sites provides us with a better alsobeen observed in othersituations (Campbell and Sloan tool to examinegypsy moth influence and facilitates com- 1977). The results described above lend credence to our parisonsbetween different studies. The studies listed in Table assertionthat increaseddefoliation associated with greater 5 eitherprovided site index measurements, or gave sufficient amountsof susceptiblespecies results in elevatedspecies informationfor usto approximatesite index. specificmortality rates and thus greater total mortality (Fig- Brownet al. (1979)used Bess et al.'s(1947) site descrip- ure 2b). tionsto characterizethe mixedstands they werestudying as either susceptibleor resistantto gypsymoth defoliation. Effect of Site Quality on Tree Mortality Thoughthey did not otherwisedistinguish between sites in Sitequality has been postulated as a primarycomponent theirarticle, the authorsprovided both the age and height of of the complexthat determinesmortality rates following dominantand codominant oaks, which allowed us to estimate gypsymoth defoliation. Attributing significance to theindi- site index for two of their studysites (Brown et al. 1979, vidualfactors that define site quality is difficult.This is due Schnur 1937). Their resultsshowed that oak mortality and in partto thefact that references to possiblerelationships to tree mortalityare often unclear;but it is also a result of totalmortality were greater on the poor quality site (SI 13 7- correlations between site conditions and resultant stand com- 15.2m) thanon the goodquality site (SI 15.2-16.8 m). This position.Localized moisture limitations may resultin some patternwas also observed by Fosbrokeand Hicks (1989) in sitesbeing dominated by xerophyticspecies that are suscep- southwesternPennsylvania, where the differencein total tible to defoliation,such as chestnut oak (Q. prinusL.) and mortalitybetween sites with SI < 18.3 m andthose with SI > scarletoak (Q. coccineaMuenchh.) (Smith, 1994). On some 21.3 m was 12%. Althoughno quantitativemeasure of site high quality sites,conifers may be excludeddue to their qualitywas given, Keggs' (1971, 1973)studies in New Jersey limited ability to competewith hardwoods,resulting in demonstrateda similar trend in mortalitydue to a gradientin susceptiblespecies dominating the site. Determining whether sitequality. mortality subsequentto defoliation can be attributedto In apparentcontradiction to thestudies described above, predefoliationsite conditions,or whetherobserved differ- someauthors have observed greater mortality rates on high encesare simply an artifact of theinfluence of siteon species qualitysites than on low qualitysites. Gansner (1987) ob- compositionis, therefore,difficult. servedthat on high (SI _>22.9 m) andmedium (SI 16.8-22.8 Referencesto possiblerelationships between site condi- m) qualitysites in centralPennsylvania, both total stand tionand tree mortality can be found throughout the literature. mortalityand oak mortalitywere greaterthan on low quahty However, in many casesa qualitativerather than a quantita- sites(SI < 16.8 m). Gansnerproposed two explanationsfor tive descriptionof sitequality was used. These descriptions his observations;the first was that on poor sitestrees were of goodand poor sites, though common, can be misleading; physiologicallybetter adaptedto endurestresses such as for instance,very dry and very wet sitesare dramatically defoliation. This is consistent with the results of Stalter and different,but they both may be described as poor. The useof Serrao(1983), whocompared mortality of northernred oak

Table 5. Mortality subsequentto gypsymoth defoliation observedwithin forest stands growing on sites of varying productivity:total mortalityis expressedas a percentageof initialstand basal area (or stemdensity); oak mortality is expressedas a percentage of initial oak basal area (or stem density). Mortality (%) SiteIndex • (m) Basisof mortalityestimate Oak Total Reference 13.7-15.2 BA 18 17 Brown et ai. 19792 15.2-16.8 BA 9 7

< 16.8 Stems 18 14 Gansner19873 i 6.8-22.8 Stems 26 21 > 22.9 Stems 28 21

< 16.8 BA 13 12 Gansner 1987 16.8-22.8 BA 23 20 > 22.9 BA 24 19

< 18.3 Stems -- 26 Fosbroke& Hicks 19894 18.3-21.3 Stems -- 16 > 21.3 Stems -- 14

1 Siteindices for Fosbrokeand Hicks(1989) are basedon equationsfrOm Wiant and Lamson(1983); all othersite indicesare based on equationsfrom Schnur (1937), 2 RhodeIsland forests, number of studyplots was not given,study period was 1971to 1975, 3 n = 574 plotsin Pennsylvania,study period was 1979to 1985, 4 n = 237 plotsin Pennsylvania,study period was 1985to 1988,

80 ForestSctence 45(1) 1999 (Q rubra L.) on dry and mesicsites and observedlower outbreakshave been observed to differ, the implication being mortalityon the dry site.The secondexplanation was that that initial outbreaksassociated with the leadingedge are secondaryagents such as Armillaria andAgrilus bilineatus moredevastating than subsequent outbreaks (Campbell 1979). areless active on poor sites. However, there does not appear Becauseit is an introducedinsect, the dearth of natural to be much evidenceto supportthis theory.In fact, the predatorsand parasites of thegypsy moth has been proposed as oppositeappears to betrue, with pathogenicity of Armillaria onereason that sustained outbreaks are more prevalent and more •ncreasingwith reductions in sitequality (Kile et al. 1991). destructivealong the leadingedge than within the generally Also, Dunbarand Stephens (1975) foundthat A. bilineatus infestedarea (McManus 1987). Othersattribute these differ- playeda majorrole in oakmortality on sites that were located encesto shifts in speciescomposition due to inter- and intraspe- ondry ridges,and upper slopes with thinrocky . A third cificvariation in susceptibilitytodefoliation (Brown and Sheals possibilityis the effect of an abnormalreduction in 1944,Campbell and Sloan 1977). The latter theory is bolstered moisture.Pennsylvania experienced several years of below by theresults of recentstudies which have demonstrated both averagerainfall duringthe early 1980s,the periodduring localadaptation to generalizedherbivory (in theform of resis- whichthe data analyzedby Gansner(1987) was collected tance),and within-population variation (family differences) in (Quimby, 1991).Trees growing on poorquality xeric sites redoak seedling response to gypsymoth defoliation (Sork et al. haveadapted to conditionsof low moistureand can tolerate 1993,Byington et al. 1994).Based on previousobservations, periodsof droughtthat would seriously impede the growth of anotherlogical explanationis shiftsin compositiondue to treesadapted to growthon high quality mesicsites (Oliver differencesin vulnerability(Campbell and Sloan 1977). During andLarson 1990, Kozlowski et al. 1991).Thus, the effects of an initialoutbreak, defoliation results in mortalityof themost this prolongedreduction in soil moisturewere probably vulnerabletrees within a stand;these are frequently suppressed much greater on the roesicsites than on the xeric sites. andintermediate individuals of susceptiblespecies, and those Consequently,defoliation on the high quality sites may have uppercanopy trees that are in poorcondition or have previously hada muchgreater than normal influence on subsequent tree experiencedsome other form of stress(Kegg 1971, Campbell mortalityduring this time period. andSloan 1977, Stalter and Serrao 1983). During subsequent While sitedifferences often appear to resultin differen- outbreaks,total stand mortality is reduced because these highly tial mortality rates,they do not follow a consistentpattern vulnerabletrees have already been removed and less vulnerable andinvolve a complexsystem of interactingfactors. Intu- individualsremain (Kegg 1971,Brown et al. 1988). itively it seemsprobable that trees on siteswith a low site Theprevious observations are borne out, in part, by the results index would suffer greater mortality than those trees of ourexamination of twogroups ofdefoliated stands (Table 6). growing on high quality sites.As we saw from the litera- We tookseveral established studies and separated them into two ture, however,the oppositeis sometimestrue. Much of groupsof predominantlyoak stands, those that could be consid- th•s inconsistencyhas been ascribedto differencesin eredinitial outbreaksand thosethat fell into the categoryof speciescomposition and physiological condition (Gansner subsequentoutbreaks. When theindividual studies within each 1987). Though treesgrowing on siteswith low site index groupwere combined, oak mortality in initialoutbreaks aver- maynot initially be asvigorous as those growing on better aged20%, whilein subsequentoutbreaks oak mortality aver- sites,some authors believe that becausethey are adapted agedonly 7%. When we testedthis difference using a two- to adverseconditions they may be better able to tolerate samplet-test (SAS 1992)it provedto be significant (P = 0.0727, defoliation-inducedstress (Stalter and Serrao 1983). Thus, t= 2.1740,df= 6).This provides strong evidence that differences when treeson high quality sitesare subjectedto drought, betweenthe two situations are due to the loss of susceptibleoaks frost, or some other perturbation,and are subsequently in initialoutbreaks. A visualexamination of totalmortality rates defoliated,these individuals suffer higherrates of mortal- indicatedthat the initial outbreaksalso experienced greater ity Other authorshave concludedthat their resultswere meantotal basal area mortality than the subsequentoutbreaks due more to site factors influencingstand composition (Table6). However,in thiscase we were unable to reject the null rather than a direct site/mortalityrelationship. Fosbroke hypothesisthat the meansof the two groupswere equal (P = and Hicks (1989) attributedtheir resultsto the fact that the 0.3027, t = 1.1646,df= 4.5). Thoughdifferences in total oak componentwas greateston poor sites. Brown et al. mortalitywere not statisticallysignificant, the resultsfrom a (1988) demonstratedthat, in three mixed standsin Rhode number of studies indicate that differences between the two Island, mortality appearedto be independentof site and situationscan be quantified. The situation described by Gansner wholly dependenton speciescomposition. The authors et al. (1993) in thePocono mountain region of Pennsylvaniais statedthat the threestand types occurred on similar sites oneexample. This area experienced two gypsymoth outbreaks (SI < 18.3 for oaks), but both oak mortality and total between1970 and 1990. The first episode(1972 to 1976) mortality were observedto increasewith increasedoak resultedin a cumulativemortality loss of 12%of the1972 stand basal area. volume.Following the second outbreak (1978-89), 10% of the TreeMortality in Initial and SubsequentOutbreaks 1978 stand volume had been killed. Cumulative volume losses A distinction is often made between areas that are on the wereestimated from 143 plots for the first outbreak and 235 plots leadingedge of thegypsy moth infestation and those that are for the second.Gypsy moth damage appraisal surveys of the in what is commonlycalled the "generallyinfested" area. stateof Pennsylvaniaprovided an opportunity to examine these While outbreaksoccur in both situations,the effects of the trendson a regionalbasis. Surveys were carded out in 1984,

ForestSctence 45(1) 1999 81 Table 6. Total mortality in predominantlyoak standsfollowing an initial gypsymoth outbreak,and following subsequentoutbreaks; total mortality is expressedas a percentage of initial stand basal area (or stem density), oak mortality is expressedas a percentage of initial oak basal area (or stem density).

Mortality (%) Standor foresttype (s) Basisof mortalityestimate Oak Total Reference Initial outbreaks Oak Stems -- 43 Kegg1973 1974 Oak BA -- 12 Gansner et al. 1993 Mixed oak BA 35 47 Campbell& Sloan1977 Mixed oak BA 18 17 Brown et al. 1979 Oak-pine BA 9 7 Brownet al. 1979 Mixed hardwood BA 17 24 Stephens& Ward 1992 Mean ' 20 21 SD 10.93 15.63

Subsequentoutbreaks Oak Stems -- 13 Gansner et al. 1983 Oak BA 13 10 Gansner et al. 1993 Mixed hardwood BA 6 15 Stephens& Ward 1992 Mixed hardwood BA 3 10 Stephens& Ward 1992 Oak-whitepine BA 6 17 Brownet al. 1988 Mean 7 13 SD 4.24 3.56 1 Mean and SD are calculatedfor BA estimatesonly. 1987, and 1990, andincluded areas that had sufferedan outbreak Observeddifferences between initial and subsequent outbreaks in the preceding3 yr period(Quimby 1991). The total area appearto be primarilyinfluenced by thepreviously described affectedby defoliationvaried considerably between surveys, relationshipbetween stand composition and tree mortality. from972,000 to 2.5 millionha. However,the portion of the Lossesof largenumbers of vulnerableoaks and lower canopy defoliatedarea that was actually affected by moderateor heavy speciesduring the initial outbreakpossibly increased stand treemortality has steadily fallen, from 17% in 1984to 11%in resistanceand reduced mortality rates during subsequent out- 1987,and finally to 2% in 1990.Quimby (1991) attributed these breaks.We cannotdiscount the possibility that selection effects differencesto above-averagerainfall during 1989 and 1990. arepre sent as well. While the studies that we reviewed were from Thereis also the possibility that a droughtduring the early 1980s differentregions, and may haveexperienced different defoha- increasedmortality during this period. As a result,while the data tionpattems, the average species specific mortality rate of those stronglysupports differences in species-specific(oak) mortal- categorizedas initial outbreakswas consistentlygreater than ity, therelationship between total mortality in initialand subse- thoseexperiencing subsequent outbreaks. Our review points out quentoutbreaks is notdefinitive. theneed for the establishment of long-term replicated studies in orderto adequatelytest some of thequestions raised here. Summary Literature Cited In conclusion,the effect of gypsymoth defoliation on tree growthand mortality continues to be of greatinterest to both BAKER,W.L. 194l. Effectof gypsymoth defoliation on certainforest trees J. For. 39:1017-1022. forestersand entomologists.Though numerous studies have beencarded out, many questions remain. There can be no doubt BAKER,W.L., At,a>A.C. CLINE.1936. A studyof thegypsy moth in thetown of Petersham,Mass., in 1935. J. For. 34:759-765. thatthe dynamics of defoliationin mixedstands of susceptible andresistant species is differentfrom thatof purestands of BEss,H.A., S.H. Seumz,At,a> E.W. LIrrLEFmLD.1947. Forest site conditaons andthe gypsy moth. Bull. No. 22.Harvard Forest, Petersham, MA. 56 p susceptiblespecies; and it appearsthat there is a directrelation- shipbetween the proportion of susceptiblespecies within a stand BLODGErr,J.T., At,a>J.J. WORP. nLL. 1992. Distributions and hosts of Annillana speciesin New York. PlantDis. 76 (2):166-170. andsubsequent tree mortality. Increasingproportions ofsuscep- tiblespecies result in greaterintensity, frequency, and duration BROWN,J.H., D.B. HALLIWELL,At,a> W.P. GOULD.1979. Gypsy moth defolla- tion:Impact in RhodeIsland forests. J. For.77:30-32. of defoliationepisodes, and thus greater total and species spe- cificmortality. In referenceto sitequality, although the studies BRowN,J.H., V.B. CROICKS.at•K,W.P. GOULD,At,a> T.P. HUSBANd.1988 Impactof gypsymoth defoliation in standscontaining white pine. North thatwe examined clearly demonstrated that total mortality rates J. Appl. For. 5:108-111. are not the sameacross all sites,the observeddifferences have BROWN,R.C., ArqD R.A.S.œALS. 1944. The present outlook on the gypsy moth notbeen consistent. Differences in mortalitydo not appear to be problem.J. For. 42:393-407. adirect result of sitequality; there is however, a strongprobabil- BYirqGworq,T.S., K.W. GorrscaALK,At,a> LB. McGRAw.1994. Within-popu- ity thatsite quality indirectly influences mortality rates through lationvariation in responseof red-oakseedlings to herbivoryby gypsy its effecton speciescomposition and thereforedefoliation. moth larvae. Am. MidL Natur. 132:328-339.

82 ForestScience 45(1) 1999 CAMPBELL,R.W. 1979.Gypsy moth: Forest influence. USDA Agric. Inf. Bull. KEcJo,J.D. 1974.Quantitative classification of foreststands as related to theft 423.44 p. vulnerabilityto loss following initial outbreak of the gypsy moth, Porthetria dispar(L.), withequations for forecasting basal area losses. M.S. Thesis, CAMPSELL,R.W., AnD R.J. Stoas. 1977. Forest stand responses todefoliation RutgersUniversity. 36 P. by thegypsy moth. For. Sci. Monogr. 19. 34 p. Kit•, G.A., G.I. McDonaLl),^ND J.W. BYLER.1991. Ecology and disease in CAMPBELL,R.W., ANDH.T. VaLEsrn•E.1972. Tree condition and mortality naturalforests. P. 102-121 in Armillaria rootdisease, Shaw,C.G. III., and followingdefoliation by the gypsy moth. USDA For. Serv. Res. Pap. NE- G.A. Kile (eds.).USDA For. Serv.Agfic. Handb. 691. 233 p. 236. 331 p. KoRs•as,C.F., ^ND A.G. Ruc,oi.•s. 1941. Report of findingsand recommen- CLE•n,rr, G.E.,AND W. MtmRO.1917. Control of thegypsy moth by forest dationswith referenceto the gypsymoth projectof the Bureauof management.USDA Agric.Inf. Bull. 484. 54 p. Entomologyand Quarantine. J. For. 39:973-979. Chow,G.R., ArmR.R. Hlcr,s, JR.1990. Predicting mortality in mixedoak KozLowsra,T.T., P.J.lCdzmaSR, •a•a> S.G. Pma.am>y. 1991. The physiological standsfollowing spring insect defoliation. For. Sci. 36(3):831-841. ecologyof woody plants. Academic Press Inc., Harcourt Brace Jovanovich, SanDiego. 657 p. DAWDSOn,C.B. 1997.Effects of Europeangypsy moth defoliation in mixed pine-hardwoodstands in theAtlantic Coastal Plain. Ph.D Diss., Virginia !Cd•usœ,S.C., ^ND K.F. Po,n:^. 1996.Differential growth and recovery rates PolytechnicInstitute and State University, Blacksburg. 213 p. followingdefoliation in relateddeciduous and evergreen trees. Trees. 10:308-316. Du•AR, D.M., • G.R. S•rmns. 1975. Association of twolined chestnut borerand shoestring fungus with mortality ofdefoliated oak in Connecti- KutMas,H.M. 1971.Effects of insectdefoliation on growth and mortality of cut. For. Sci. 21:169-174. trees. Ann. Rev. Entomol. 16:289-324.

DUNN,J.P., T.W. KIMMERER,AND G.L. NORDIN.1986. Attraction of the LIEBHOLD,A.M., œTaL.. 1995.Suitability of NorthAmerican tree species to twolinedchestnut borer, Agrilus bilineatus (Weber) (Coleoptera: thegypsy moth: A summaryof field andlaboratory tests. USDA For. Buprestidae),and associatedborers to volatilesof stressedwhite oak. Serv.Gen. Tech. Rep. NE-211.45 p. Can. Entom. 118(6):503-509. LIESHOLDA.M., W.L. M^cDonaLD,D. BERaD^m.,^ND V.C. Mastro. 1994. Invasionby forestpests: A threatto forestecosystems. For. Sci. Monogr. Du•, J.P., T.W. IOMM•P.•R,ANl) D.A. Po•'rER.1987. Winter starchreserves 30:1-49. of white oak as a predictorof attackby the twolinedchestnut borer, Agrilusbilineatus (Weber) (Coleoptem: Buprestidae). Oecologia. 74: 352- McM^nus,M.L. 1987.The gypsy moth problem: History, biology, spread. P. 355. 1-10 in Proc.,Coping with the gypsymoth in the new frontier:A workshopfor forestmanagers. Fosbroke, S., and R.R. Hicks(eds.). West Dl)•, J.P.,D.A. Po•rsR,• T.W.ICaMMERER.1990. Carbohydrate reserves, Virginia Univ. Books,Morgantown. 153 p. radialgrowth, and mechanismsof resistanceof oak treesto phloem- boringinsects. Oecologia. 83:458-468. Minorr, C.W., ^NDI.T. Gl)nD. 1925. Someresults of the defoliationof trees. J. Econ. Entomol. 18:345-348. Fo•usH, E.H., • C.H. FERnaLl).1896. The gypsymoth. Wright & Potter, Boston.495 p. MONTGOMERY,M.E. 1991.Variation in thesuitability of treespecies for the gypsymoth. P. 1-13 in Proc. U.S. Dep. of Agfic. Interagency Gypsy Moth FOSBROKE,D.A., aNDR.R. H•cr,s, JR. 1989. Tree mortality following gypsy Res.Rev. 1990. Gottschalk,K.W., et al. (eds.).USDA For. Serv.Gen. mothdefoliation in southwesternPennsylvania. P. 74-80 in Proc.7th Tech.Rep. NE-146. 152 p. Cent.Hardw. For. Conf., Rink, O., and C.A. Budelsky (eds.). USDA For. Serv.Gen. Tech. Rep. NC-132. MOr½r•OMER¾,M.E., AND W.E. WaLLr•raz. 1988. The gypsy moth: A westward migrant.P. 353-375in Dynamicsof forestinsect populations, patterns, G•S•ER,D.A. 1987.Site productivity and tree mortality on new frontiers of causes,implications. Berryman, A.A. (ed.).Plenum Press, New York and gypsymoth infestation. USDA For.Serv. Res. Note. NE-340. 3 p. London. G^ns•ER,D.A., O.W. FIERPaCœ,P.S. Dr;BaLl),^ND R.E. ACC•^VATn.1983. MosttaR,F.H. 1915.Food plants of the gypsy moth in America.USDA Agric. Changesin forestcondition associated with gypsy moth. J. For. 81(3):155- Inf. Bull. 250. 39 p. 157. NICHOLS,J.O. 1968.Oak mortality in Pennsylvania.J. For. 66:681-694. G^ns•ER,D.A., S.L. Am,w.a, R.H. WinMash,^ND C.L. ALdRiCH.1993. After OLIVE•,C.D., ANDB.C. LA•SOn.1990. Forest stand dynamics. McGraw-Hill, two decadesof gypsymoth, is thereany oak left? North. J. Appl.For. New York. 467 p. 10(4):184-186. PARr,ER, J. 1981.Effects of defoliationon oak chemistry. P. 219-225in The Oorrsc•c, K.W. 1993.Silvicoltural guidelines for forest stands threatened gypsymoth: Research toward integrated pest management, Doane, C.C., bythe gypsy moth. USDA For. Serv. Oen. Tech. Rep. NE-171.50 p. andM.L. McManus(eds.). USDA For. Serv.Tech. Bull. 1584.757 p. Gorrsc•œ, K.W., ^NDM.J. TWER¾. 1989. Gypsy moth impacts in pine- PARr,FaZ, J., ANDD.R. HOUSTOn.1971. Effects of repeateddefoliation on root hardwood mixtures. P. 50-58 in Proc. Pine-Hardwood Mixtures: A androot collar extractives of sugarmaple trees. For. Sci. 17(1):91-95. Symp.on Managementand Ecology of theType, Waldrop, T.A. (ed.). USDAFor. Serv.Gem Tech. Rep. SE-58. QUIMBY,J.W. 1991.Tree mortality following gypsy moth epidemics--1990. PennsylvaniaBureau of Forestry,Division of ForestPest Management H^Rx,J.H. 1990.Effect of gypsymoth on aspen in Michigan.P. 173-176in Report.50 p. Proc.1989 Aspen Symp., Adams, R.D. (ed.)USDA For.Serv. Gem Tech. Rep. NC-140. SAS INST•TtJ•. 1992. SAS/STAT© Users Guide Volume 2, GLM- VARCOMP,Version 6, Fourthedition. SAS Institute, Cary, NC. P. 891- Hol)ston,D.R. 1981.Mortality and factors affecting disease development. P. 996. 281-293in Thegypsy moth: Research toward integrated pest manage- ment,Doane, C.C., andM.L. McManus(eds.). USDA For. Serv.Tech. ScHnuR,G.L. 1937.Yield, stand, and volume tables for even-aged upland oak Bull. 1584.757 p. forests.USDA Tech.Bull. 560. 87 p. Houston,D.R., mm H.T. V^rr•m•E.1977. Comparing and predicting forest SCHOWaL•R,T.D., W.W. I-•R•ROVE,AND D.A. CROSSt.E¾,JR. 1986. Her- standsusceptibility to gypsy moth. Can. J. For.Res. 7:447-461. bivoryin forestedecosystems. Ann. Rev. Entomol.31:177-96. Houston,D.R., ^ND H.T. VaLssm•E.1985. Classifying forest susceptibility SMIT•,D.W. 1994.The southern Appalachian hardwood region. P. 173-225 to gypsymoth defoliation. USDA Agfic. Handb. 542. 19 p. in Regionalsilviculture of the UnitedStates. Ed. 3. Barrett.J.W. (ed). Wiley,New York. KEc,o, J.D.1971. The impact of gypsymoth: Repeated defoliation of oakin New Jersey.J. For. 69:852-854. SoR•c,V.L., K.A. STOWE,AnD C. HOCHWENDER.1993. Evidence for local adaptionin closelyadjacent subpopulations of northernred oak KEcJo,J.D. 1973. Oak mortality caused by repeated gypsy moth defoliations (Quercusrubra L.) expressedas resistanceto leaf herbivores.Am. In New Jersey.J. Econ.Entomol. 66(3):639-641. Natur. 142(6):928-936.

ForestScience 45(1) 1999 83 STALEY,J.M. 1965.Decline and mortality of redand scarlet oaks. For. Sci. WARGO,P.M. 1977.A rrnillariella rnellea and Agrilus bilineatus and mortality 11(1):2-17. of defoliatedoak trees.For. Sci. 23(4):485-492.

STALTER,R., ANDJ. S•RRAO.1983. The impactof defoliationby gypsymoths WARGO,P.M. 1981a. Defoliation and secondary-actionorganism attack on the oak forestat GreenbrookSanctuary, New Jersey.Bull. Tort. Bot. With emphasison Arrnillaria rnellea. J. Arbor.7(3):64459. Club. 110(4):526-529. WARGO,P.M. 1981b.Defoliation and tree growth. P. 225-240 in The gypsy STE•'•NS,G.R. 1988.Mortality, dieback and growth of defoliatedhemlock moth:Research toward integrated pest management, Doane, C.C., and andwhite pine. North. J. Appl. For. 5:93-96. M.L. McManus(eds.). USDA For. Serv.Tech. Bull. 1584.757 p. ST•I'•NS, G.R., ANDJ.S. WARD.1992. Sixty yearsof naturalchange in WARGO,P.M., ANOD.R. HOUSTON.1974. Infection of defoliatedsugar maple unmanagedmixed hardwoodforests. Conn. Agric. Exp. Sta. Bull. treesby Arrnillariarnellea. Phytopathology 64:817-822. 902.63 p. WARGO,P.M., AN•T.C. I-IAmZlNGWON.1991. Host stress and susceptibility P TIONœR,T. 1992.Gypsy moth impact on Virginia'shardwood forests and 88-101 in Armillariaroot disease, Shaw, C.G. Ill., andG.A. Kile (eds) forestindustry. Virginia Dep. of For., Charlottesville,VA. 36 p. USDA For. Serv.Agric. Handb. 691. 233 p. TWER¾,M.J. 1991.Effects of defoliationby gypsymoth. P. 27-39 in Proc. WAXLING,R., G.A. KILE, ANDH.H. BURDSA•.•.,JR. 1991. Nomenclature, U.S.Dep. of Agric. Interagency Gypsy Moth Res. Rev. 1990. Gottschalk, , and identification. P. 1-9 in Armillaria root disease, K.W., et al. (eds.).USDA For. Serv.Gen. Tech. Rep. NE-146. 152p. Shaw, C.G. Ill., and G.A. Kile (eds.). USDA For. Serv. Agnc Handb. 691. 233 p. TWERY,M.J., G.N. MASON,P.M. WARGO,At, a) K.W. Go•rSCHALK.1990. Abundanceand distribution of rhizomorphsofArmillaria spp. in defoli- WiArqr,H.V. JR.,A•a) N.I. LAMSON.1983. Site index equations for even-aged atedmixed oak stands in westernMaryland. Can. J. For. Res. 20:674-678. oak standsin northwesternWest Virginia. For. Notes 10:11-12. WARO0,P.M. 1972.Defoliation-induced chemical changes in sugarmaple rootsstimulate growth of Armillariareellea. Phytopathology. 62:1278- 1283.

84 ForestScience 45(1) 1999