United StatesDepartment ofAgriculture

Forest Service

Southeastern ForestExperiment Station

General TechnicalReport SE-55

An Overview of thePine Wood Nematode Banin North America

.

L.D. Dwinell

W.R. Nickle

North AmericanForestry CommissionPublication No. 2

May 1989

Southeastern Forest Experiment StationF?O. Box 2680

Asheville, North Carolina 28802

An Overview of the Pine WoodNematode Ban in North America

L. D. Dwinell, Principal Research Plant PathologistSoutheastern Forest Experiment StationForestry Sciences LaboratoryAthens, Georgia

W. R. Nickle, Research NematologistUSDA Agricultural Research ServiceSystematic Botany, Mycology, and Nematology LabBeltsville, Maryland

ABSTRACT

The history, ecology, and biology of the Bursaphelenchus-Monochamus complex in North America are reviewed. The pinewood nematode (B. xylophius) is a secondary associate of nativeconifers and the most common mode of transmission is duringoviposition of the Monochamus vector. The pine wood nematodeis a primaty pathogen of exotic pines, however. Primary andsecondary transmission of B. xylophilus are described. Since thenematode is seldom a primary pathogen in North America,distribution there cannot be equated with the distribution of thepine witl disease. Recent research on the incidence, control, andrisks of the pine wood nematode and its vectors in exported softwoodproducts is reviewed.

Keywords: Bursaphelenchus xylophilus, Bursaphelenchus mucrona-tus, Pinus, embargo, softwood products, Monochamus, pine wiltdisease.

Embargo

Recent events have focused new attention onthe status of the pine wood nematode, Bursaphe-lenchus xy/ophi/us (Steiner & Buhrer) Nickle (= B.lignicolus Mamiya & Kiyohara), in North America. In1984, pine chips headed for Finland from the UnitedStates (fig. 1) and Canada were found to be infestedby pine wood nematodes (Rautapaa 1986). Sincethis nematode was considered to be the causalagent of pine wilt disease (Mamiya 1988, 1984)Finland in 1985 banned importation of conifer chipsand timber cut from softwood trees grown in areasof the world in which the pine wood nematode occurs(Rautapaa 1986). The other Scandinavian countriesfollowed suit. In July 1985, the European PlantProtection Organization (EPPO) recommended thatEurope as a whole ban softwood products exceptkiln-dried lumber from countries known to have B.xy/ophi/us (Smith 1985).

These events resulted in a rapid exchange ofinformation between the countries concerned. Fact-finding teams from Finland, Norway, and Swedenvisited the United States and Canada. The ban hasbeen costly to the forest industries in North America.Understandably, however, the importing countriesare concerned about the health of their forests anddo not want to experience a pine wilt disease epidemicsuch as has occurred in Japan (Mamiya 1988, 1984).They must evaluate the magnitude of the problem inJapan, the problem on Scotch pine in the MidwesternUnited States, and the possible threat to the forestsof Nordic and other European countries. Recentdiscussions with European scientists and governmentofficials suggest that the current status of the pinewilt disease in North America is not fully understoodthere. For example, the opinion has been expressedthat some exported pine chips are from trees killedby a pine wilt epidemic in North America. One of themain arguments put forth by Rautapaa (1986) ofFinland was that ‘the nematode has caused significanteconomic damage to pines in USA and in Japan.’EPPO (1986) stated that the pine wood nematode isassociated with tree dieback in Canada. In fact, pinewood nematodes are seldom, if ever, the primarycause of mortality of conifers in the forests of NorthAmerica.

New Perspectives on Past Research

Research on a pest such as the pine woodnematode is a dynamic process. Each new discoveryprovides fresh insight, which sometimes changesone’s perceptions of the pest and the disease itcauses, and requires a critical reevaluation of theprevious literature. Scientists in a network that activelyexchanges information frequently recognize the subtlechanges in direction before the scientific communityat large. Unfortunately, the significance of suchdiscoveries is not always fully appreciated.

This report examines some new observations onthe pine wilt disease complex. It places the currentstatus of the pine wood nematode and the pine wiltdisease in North America into perspective. ‘Perspec-tives; as Van Gundy (1986) noted, ‘are the way wesee and interpret things based on our own experienceand individual philosophies.”

Initial Reaction to Rediscovery of PineWood Nematode in North America

The pine wood nematode (as B. lignicolus) wasfirst reported from North America in 1979. It wasfound on dead Austrian (Pinus nigra Arnold) andScotch (P. sylvesfris L.) pines in Missouri (Dropkinand Foudin 1979), and was thought to have beenintroduced from Japan. The initial reaction by thescientific community, reflected in the literature of thetime, was ‘We’ve been invaded!” (Hoideman 1980).In 1981 B. lignicolus, the Japanese nematode, wassynonymized with B. xy/ophi/us (Nickle and others1981), a species known to occur in North America.Earlier, Nickle (1970) had transferred Aphelenchoidesxylophilus Steiner & Buhrer to Bursaphelenchus.Aphelenchoides xylophilus had been found in associa-tion with fungi in downed timber (Steiner and Buhrer1984). Although the pine wood nematode has beenknown to be in North America for at least 60 yearsand is probably a native species, research in theUnited States has continued to emphasize pathogene-sis. In a thorough evaluation of the problem, Holdeman(1980) concluded that the pine wood nematode wasnot a threat to conifers in California. Some landmarksin the history of research on the pine wood nematodeare outlined in table 1.

Relationship of Bursaphelenchus WithMonochamus

Most of the 49 described species of Bursaphe-lenchus have a phoretic relationphip with insects,especially bark beetles and wood borers, $nd all are ,f, ,

The biologies of the Asian, North American, andEuro-Siberian Monochamus species are similar.Species differ in geographical distributions, hostplants, oviposition site preferences (location on trunk,mycophagous (Massey 1974; Rijhm 195 . The pine ‘I’ ti

wood nematode and other closely relatzspecies of * )Ietc numbers of instars, and length of life cycle

Bursaphelenchus are vectored principally by ceramby- (Hellrigl 1971; Kobayashi and others 1984; Linit 1987;

cid longhorn beetles (also referred to as sawyers) in Linsley and Chemsak 1984; Webb 1909).

species similar to B. xy/ophi/us, may be the aboriginalinhabitant of M. akernatus in Japan (Mamiya 1988;Mamiya and Enda 1979).

In the United States, dauerlarvae of B. xy/ophi/ushave been recovered from adult beetles of M.carolinensis Oliver, M. scutellatus Say, M. titilkorFabricus, M. muraror LeConte, M. scutellatus orego-nensis (LeConte), and M. nofafus Drury (Holdeman &&Q1980; Linit and others 1988;I(Uickle and others 1980; 1 f@y-Tarjan and others 1980; Wingfield and Blanchette1988. A possible strain of 8. xy/ophi/us in which theadult females have mucronate tails similar to thoseof B. mucronafus is phoretic on M. marmorator andM. scurellafus (Wingfield and Blanchette 1988).

In Canada, 14 potential insect vectors of thepine wood nematode are known to be present(Garland 1985). These include six species of longhornbeetles: M. carolinensis, M. marmorafor, M. mutator,M. obtusus Casey, M. scutellafus, and M. titillator.Bursaphelenchus xy/ophi/us was first reported inCanada in 1988 (Knowles and others 1988).

Research in Mexico on longhorn beetles hasbeen limited. Monochamus nofafus has been reportedon Pinus spp. and Abies spp. in Mexico State, andM. rubigineus Bates (= M. clamafor rubigineus (Bates)Linsley & Chemsak) have been found on P. pa&/a inHidalgo State (Samaro 1987). Reportedly, M. clamatorrubigineus has a range from southeastern Arizona toHonduras, and the host plants include P. leiophyllaSchiede & Deppe and P. ponderosa Dougl. ex Laws.(Linsley and Chemsak 1984). Samano (1987) howev-er, believes that several other species of Monochamus,including known vectors of the pine wood nematode,occur in Mexico. Although B. xylophilus has not beenreported in Mexico, its existence there is highlyprobable.

the genus Monochamk. These beetles are saprophyt-ic wood borers in the larval stage (Hellrigl 1971; Linit1987; Webb 1909).

In Japan, China, and Taiwan, M. alternatus Hopeis the primary vector of B. xy/ophi/us (Mamiya 1987;Mamiya and Enda 1972). Monochamus nifens Bates& M. saltuarius Gebler are also considered to bevectors in Japan (Kobayashi and others 1984).Bursaphelenchus mucronarus Mamiya & Enda, a

The adult sawyers are attracted to recently deador dying trees and freshly felled timber (includinglogs) for breeding. The cause of the conifer’s mortalityis not particularly significant. In the United States, forexample, sawyers breed in pines killed by otherinsects such as the southern pine beetle (Dendroc-tonus frontalis Zimm.) (Coulson and others 1976;Dwinell 1988) or the engraver beetle (Ips calligraphusGerm.) (Miller 1984), by root rot and drought (Dwinell

Table 1. -Some landmarks in the history of pine wood nematode research

Year Event Reference

1909

1929

Biology of Monochamus ririlaror described Webb 1909

@he/enchoides xy/ophi/us found in association withfungi in timber Steiner and Buhrer 1934

1969 Bursaphelenchus sp. found in wood of deadpine trees in Japan Tokushige and Kiyohara 1969

1970 Aphelenchoides xy/ophilus transferred toBursaphelenchus Nickle 1970

1971 Pathogenicity of Bursaphelenchus sp. demonstratedby inoculating 25year-old Pinus densiflora Kiyohara and Tokushige 1971

1972 Pine wood nematode described as B. lignicolus Mamiya and Kiyohara 1972

Transmission of B. lignicolus by Monochamusalrernarus reported (maturation feeding) Mamiya and Enda 1972

1979 Bursaphelenchus mucronarus is described Mamiya and Enda 1979

Pine wilt disease reportedly found in the UnitedStates Dropkin and Foudin 1979

1981 Bursaphelenchus lignicolus placed as a synonymof B. xylophilus Nickle and others 1981

1983

1984

Transmission of B. xy/ophi/us during ovipositionof Monochamus vectors reported Wingfield 1983

Bursaphelenchus xy/ophi/us found in Canada Knowles and others 1983

Bursaphelenchus xylophilus intercepted in pinewood chips imported into Finland from theUnited States and Canada Rautapaa 1986

1987b; Highley and others 1982) by dwarf mistletoe(Arceuthobium americanurn Nutt.) (Burnes and others1985), or by flooding (Esser and others 1983). Sawyersalso attack fire-damaged, blown-down, or lightning-struck trees (Hellrigl 1971; Webb 1909). An exceptionis M. marmoraror Kilby, which attacks standing greenbalsam fir (Abies balsamae (L.) Mill.) and hastens thedeath of trees weakened from other causes (Craig-head 1960).

The bark must still be on the tree or log for beetlesto oviposit and for the insect larvae to develop(Craighead 1950; Hellrigl 1971; Webb 1909). Thefemale gnaws an irregular hole through the bark

(oviposition pit) and inserts from one to six eggs.Nematodes can be transmitted at this time. The larvafeeds from 1 to 2 months on the cambial-fiber layer,consuming all cambial and soft bark tissues. Theentire bark is loosened from the wood and the spaceis packed with excelsior and frass. Later, the larvabores into the sapwood forming an oval entrancehole. The tunnel is usually U-shaped, and the pupalcell is in the sapwood just beneath the outer bark.After pupation, the adult emerges by gnawing throughthe bark. In the more northern parts of the ranges, 2years are required to complete the life cycle (Hellrigl1971; Linit 1987; Webb 1909).

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Ecologically, the life cycles of the cerambycidvector and the pine wood nematode are well integrat-ed. The nematodes have distinct life cycles forpropagation and dispersal. The propagative nematodemay feed on the epithelial cells of the resin ducts(phytophagous) or on the fungi that invade the wood(mycophagous). The dispersal cycle takes placeduring times of stress, such as when the woodbecomes dry after tree death or in the late fall. Thenonfeeding third larval dispersal stage is adapted tosurviving unfavorable conditions (Mamiya 1983, 1984;Wingfield 1987; Wingfield and others 1984).

In the presence of the callow adult (pupa) of thevector (fig. 2) the third larval dispersal stage moultsto the fourth larval stage, which is referred to as theVansmission stage’ or ‘dauerlatva: Up to as manyas 100,000 dauerlarvae may enter the callow adult ofthe insect through the thoracic spiracles and areheld in a quiescent state only in the tracheae.Dauerlarvae are adapted to being carried by theinsect vector to a new habitat (Linit 1987; Mamiya1983, 1984; Wingfield and others 1984). However,not all sawyers become infested by B. xy/ophi/us. Forexample, Kinn (1987) found that 31.4 percent of the

Figure 2.-The pupa (callow adult) of the pine sawyer may becomeinfested with the dauerlarvae of Bursaphelenchus sp. Shown hereis a pupa of Monochamus titillator, the southern pine sawyer.

Ad. titillafor and 50 percent of the M. carolinensisrecovered from barrier traps carried dauerlarvae ofthe pine wood nematode.

Upon emergence, the adult beetle moves to asuitable live host to feed on the bark of young branches(Kobayashi and others 1984; Linit 1987; Mamiya1983, 1984) (fig. 3). Nematode dauerlarvae emigratefrom the spiracles and enter the tree through woundscaused by maturation feeding (Mamiya and Enda1972). This mode of transmission is termed ‘primary’

Figure 3.-Primary transmission occurs during maturation and subsistence feeding of pine sawyers on shoots of susceptible speciesof pine.

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because primary infection of an apparently healthytree occurs (Linit 1987). Once within the stressedtree, the nematode reproduces rapidly and theinfected tree shows symptoms of decline and wilt(Kobayashi and others 1984; Linit 1987; Mamiya andEnda 1972). If these events occur, the nematode isfunctioning as a primary pathogen and the resultantdisease is known as pine wilt.

Pathogenicity of B. xy/ophi/us to NorthAmerican Pines

Much of the information about pathogenic@ ofthe pine wood nematode in North America is basedon seedling pathogenicity tests. Misinterpretation oftest results may have contributed to the impressionthat the pine wilt disease is epidemic in North America.Pathogenicity on inoculated pine seedlings does notimply pathogenicity on established trees (Bedker1987; Wingfield 1987; Wingfield and others 1984).Bedker (1987’) cites numerous studies which suggestthat seedling mortality in tests does not indicate thatB. xylophilus can kill trees in the field. Also, manyscientists in North America have conducted unsuc-cessful.field pathogenicity tests with the pine woodnematode. Because the results were negative, theyoften were not published. For example, slash pine(P. elliottii Engelm. e//iottii) seedlings can be killedby B. xylophilus in greenhouse inoculations (Dwinell1985; Luui and Tarjan 1982) but Dwinell’s boleinoculations in 1986 on 16year-old slash pines (upto 105 nematodes/bole) during the worst drought onrecord in Georgia resulted in no disease developmentand these results were not published. As Wingfieldand others (1984) noted, ‘Inoculation of seedlings inthe greenhouse only provides clues to what may behappening in the forest’. The inferences that can bemade from greenhouse seedling inoculations aregenerally limited to the conditions under which thestudies were conducted.

Based on field pathogenicity tests in which theinoculation procedure approached the natural infec-tion process and satisfied Koch’s postulates, onlyScotch (Bedker and Blanchette 1984), slash (Luuiand others 1984) Japanese red (P. de&flora Sieb.8 Zuc.), and Japanese black (P. fhunbergii Parl.)(Mamiya and Enda 1979) pines currently should beconsidered suscepts of the pine wood nematode.That is, susceptibility to the pine wilt disease in naturehas been satisfactorily demonstrated only on thesefour pines. Because of high inoculum density and an

inoculation procedure that did not fully mimic matura-tion feeding by pine sawyers, the study reported byBedker and Blanchette (1988) for Scotch pine is notdefinitive. In a similar study, shoot inoculations withpine wood nematodes resulted in dieback but not intree mortality (Bedker and others 1987). Luzzi andothers (1984) demonstrated pathogenicity onlo-year-old field-grown slash pines in Florida whenthe nematodes were transmitted to the host by M.titillafor Fabricus. Luzzi and Tarjan (1982) however,reported that no infection occurred when branchesof lo-year-old slash pines were artificially inoculatedwith up to 25,000 B. xy/ophi/us. Of the four pine specieswith proven susceptibility, only slash pine is native toNorth America. However, mortality of slash pine treesdue to the pine wilt disease is extremely rare. Untilproved otherwise by field pathogenicity tests thatmimic the natural infection process, conifers nativeto North America should be considered to be immuneor highly resistant to the disease. The classificationof conifers as ‘resistant’ or ‘susceptible’ to 13.xylophilus, based on greenhouse seedling tests orfield inoculation procedures that do not simulate thenatural infection process, is artificial.

Implications of Secondary Transmission

The pine wood nematode is transmitted to deador dying pines during oviposition. Secondary transmis-sion, first reported by Wing-field in 1988, occurs whenB. xyiophilus enters the tree through ovipositionwounds. This mode of transmission has beenconfirmed (Luui and others 1984; Wingfield andBlanchette 1988) and is now considered the mostcommon means of transgenerational transfer ofspecies of Bursaphelenchus. The realization thatBmaphe/enchus is transmitted during ovipositionessentially redefined the status of the pine woodnematode in North America (Wingfield and others1984). This revelation requires that the previousliterature on the nematode be critically reevaluatedtaking secondary transmission into consideration.For example, if oviposition pits are noted on dead ordying pines, and the nematode is isolated, it cannotbe automatically inferred that the tree succumbed tothe pine wilt disease. Numerous studies since 1988have demonstrated that the nematode is a secondaryassociate of the tree in these cases and does notcontribute to tree mortality (Bedker 1987; Burnesand others 1985; Dwinell 1987b; Wingfield andBlanchette 1988; Wingfield and others 1982). AlthoughWingfield presented his hypothesis on transmissionduring oviposition in 1982, major review articlespublished as late as 1985 (except Wingfield and

others 1984) do not refer to secondary transmission.In the development of a hypothesis on the distributionof the pine wilt disease with respect to temperature,Rutherford and Webster (1987) did not fully considersecondary transmission. The EPPO (1986) publicationthat defines B. xylophilus as a quarantine organismdoes not mention secondary transmission.

The Two Forms of Bursaphelenchus IsolatesFrom North America

Currently, North American isolates of t3. xylophilusare referred to by some as one of two forms: ‘R”(round tail) and ‘M’ (mucronate tail). The ‘R” fo7m isconsidered the causal agent of the pine wilt disease.

The Monochamus-BursaphelenchusComplex Outside North America

In assessing the risk of the pine wood nematodein exported softwood products, it is also necessaryto look briefly at the Monochamus-Bursapbelenchuscomplex in Europe. Unfortunately, criiical informationis lacking on possible associations of species ofBursaphelenchus with the European species ofMonochamus (for example, M. sartor F., M. sutor L.,and M. galloprovincialis Oliv.). Bursaphelenchussuforicus Devdariani (Devdariani 1974) and B.kolymensis Korentchenko (Korentchenko 1980) havebeen described and are phoretic in M. sutor, a speciesof Monochamus found in northern Scandinavia,Finland, and throughout central Europe (Hellrigl1971). The range of B. sutoricus and B. kolymensisin relation to M. sufor has not been determined. Thebiology and pathogenic potential of 6. suroricus andB. kolymnensis have not been studied. B. mucronafushas been found from M. sufor in Sweden and thisBursaphelenchus-Monochamus complex is currentlybeing studied by Swedish scientists (Magnussonand others 1988).

De Guiran and others (1986) noted that, ‘thetaxonomic situation of B. xy/ophi/us and relatedspecies is rather puzzling.’ In 1979, Mamiya andEnda described B. mucronatus from wood of Japanesered pine in Japan. This new nematode is similarmorphologically to B. xy/ophi/us but has a distinctmucro at the tail terminus in females and larvae (fig.4). Mamiya (1986) reported that crosses of theJapanese isolates of B. xy/ophi/us and B. mucronatusdo not produce fertile offspring. The validity of B.mucronarus was questioned by Baujard (1980) whosynonymized it with B. xylophilus. This change,however, has not been accepted. Bursaphelenchusmucronarus have also been taken from Scotch pinein Norway (McNamara and others 1988). Schauer-Blume (1987) found a nematode similar to B. mucrona-rus (=B. fraudulentus (Ruhm 1956)) in dying or deadoak (Quercus), cherry (Prunus), and beech (Fagus)trees in West Germany.

Wingfield and others (1983) isolated from balsamfir nematodes whose adult females had mucronatetails similar to those of B. mucronarus. The nematodewith the mucronate tail mated with B. xy/ophi/us frompine but not with B. mucronarus from Japan.

Wingfield and Blanchette (1983) report that the‘M’ form of 6. xylophilus is phoretic in M. marmoratorand M. scurellarus. Balsam fir is the exclusive host ofM. marmorator (Craighead 1950; USDA FS 1985)whereas M. scurellarus is found on many conifersincluding species of Pinus, Abies, Larix, and Picea(Linsley and Chemsak 1985). The ‘M’ form of B.xy/ophilus from balsam fir may therefore not berestricted to balsam fir (Wingfield and Blanchette1983). In Canada, for example, the “M” form hasbeen reported from balsam fir, black spruce (ficeamariana (Mill.) B.S.P.), eastern white pine (Pinussrrobus L.), red pine (P, resinosa Ait.), and jack pine(P. bankdana Lamb.). The ‘R” form has been isolatedfrom red and jack pines (Canadian Forestry Service1985). Both forms were found in single trees. Thedistribution of the ‘M’ and ‘R’ forms is probably dueto preference of the nematode and host preferencesof species of Monochamus. It is currently our opinionthat the ‘M’ form of B. xy/ophi/us is part of a B.mucronatus complex and is not a true strain of thepine wood nematode.

Baujard and others (1979) reported the presenceof 8. xy/ophi/us in France. The French strain has themucronate female tail of 6. mucronatus but canhybridize with both ff. xy/ophi/us and B. mucronatus(De Guiran and Boulbria 1986). Enzyme electrophore-sis has shown phenotypic differences among B.xy/ophi/us, B. mucronatus, and the French strain.The French strain may be intermediate between B.xy/ophi/us and B. mucrortarus (De Guiran and others1985). On the basis of this research in France,Rutherford and Webster (1987) concluded that pinewilt disease is present in Europe.

Many gaps in our knowledge of the taxonomy ofBursaphelenchus cloud an international perspectiveof the problem. For example, no information is availableon what insects (i.e., Monochamus spp.) are associat-ed with the French strain. However, the ‘R’ form ofthe nematode is the culprit and its distribution is ofprimary concern.

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Figure 4.-Scanning electron microscope pictures. A. Front end, female lip region of 6. xy/ophi/us. B. Male, tail of B. xy/ophi/usshowing typical spicule, caudal alae, and papillae. C. Female tall end, B. mucronafus showing distinctive mucron at tip of tail. D.Female tail end, 6. xy/ophi/us showing rounded tail tip.

Bursaphelenchus xylophilus Not Synony-mous With Pine Wilt Disease

The literature shows a marked tendency to treatB. xylophilus and the pine wilt disease as the sameentity. They are not! Although the pine wood nematodeis the causal agent of the pine wilt disease, it normallyexists in nature independent of the disease. Thus,the distribution of B. xy/oohi/us cannot be equatedwith the distribution of pine wilt disease in NorthAmerica. Because of secondary transmission, B.xylophilus can be expected to be found throughoutNorth America wherever recently killed or dyingconifers are colonized by species of Monochamus.Also, in Canada and the Northern United States onewould expect to find both the so-called R and Mforms (Canadian Forestry Service 1985; Wingfieldand Blanchette 1983; Wingfield and others 1983).The so-called M form has not been reported fromthe southern pines.

From 1979 to 1982, Robbins (1982) compiledreports of the pine wood nematode from across theUnited States. She emphasized ‘that these reportsdeal with trees from which pine wood nematodeshave been extracted and not with reports of pine wiltdisease.’ These data have frequently been usederroneously to infer that the pine wilt disease iswidespread in the United States and involves severalconifer species.

In North America, the pine wilt disease appearsto be limited primarily to stressed exotic pines-namely, Scotch, Austrian, Japanese red, and Japa-nese black pines. Of these four pines only Scotchpine has been demonstrated to be a possible susceptin North America by field pathogenicity tests (Bedkerand Blanchette 1988). Scotch pines have been plantedextensively in North America as ornamentals, wind-breaks, and Christmas trees. Losses normally followsummers with above-average temperatures anddrought conditions (Malek and Appleby 1984). It isnot clear from available data what percentage of theScotch pines that have died since 1979 have actuallysuccumbed to the pine wilt disease. For example,Malek and Appleby (1984) noted that cerambycidbeetles often began ovipositing in dying trees beforethe onset of foliar symptoms. It is possible that manyof the Scotch pines were dying for reasons otherthan pine wilt (i.e., root rot (Horner and others 1987;Highley and others 1982)) and that the pine woodnematode had been transmitted during oviposition.Further field studies are needed to show the fullsignificance of the pine wood nematode in the mortalityof Scotch pine. We feel the whole situation with Scotchand other exotic pines needs to be reevaluated.

Mamiya (1984) states that in Japan high tempera-tures and dry growing seasons greatly favor theintensification and spread of pine wilt. The heaviestannual loss in volume and number of pine trees wasrecorded in 1978 in Japan and was attributed to anunusually hot and dry summer. Takeshita and others(1975) demonstrated that low summer precipitation(less than 30 mm during 40 days of the summerseason) and high temperatures (more than 55 dayswith a mean daily temperature above 25 % throughoutthe season) were highly responsible for the incidenceof severe damage. Dwinell (1986), furthermore,reported the optimum temperature for the reproduc-tion of the pine wood nematode in wood chips wasabout 35 “C. The Nordic countries seldom have thisdegree of heat and drought.

Scientists are concerned that changing forestmanagement practices could result in the increasedincidence of diseases such as pine wilt, The pinewood nematode may have been responsible for themortality of slash and sand (P. clausa (Chapm. exEngelm.) Vasey ex Sarg.) pines in seed orchards inFlorida in the early 1980’s (Blakeslee and others1987). Pathogenicity was not demonstrated, however.The pine wood nematode was associated with dyingVirginia pines (P. virginiana Mill.) in a progeny test inGeorgia and in a seed orchard in Alabama, but wasprobably a secondary invader of these dying pines(Dwinell and Barrows-Broaddus 1983). In a study ofmortality of sand pine in a seed orchard in centralGeorgia, it was concluded that B. xylophilus was asecondary associate and did not contribute to treemortality (Dwinell 1987b). Except for a few isolatedcases, there is no evidence that pine wilt disease isa problem on southern pines.

The spread and development of the pine wiltdisease to epidemic proportions in Japan suggeststhat the pine wood nematode was introduced intoJapan. Since B. xylophilus is widespread in NorthAmerica, it has been speculated that it originated inNorth America (Mamiya 1983, 1987). This hypothesisis not supported by experimental data and is currentlybeing questioned. It has been suggested that bothM. akernatus and B. xylophilus came to Japan fromChina and that the sawyers were free of nativeparasites and therefore more vigorous and thepopulations built up to very large numbers (up to60,00O/hectare). Whatever its origin, the nematodeprobably entered Japan in some form of raw softwoodproduct (i.e., unbarked logs). The only documentedcase of transfer of pine wilt occurred in Okinawawhen infested logs were brought in from Japan tobuild a pier, and vector beetles emerged and spreadthe nematode to nearby stands of luchu pines (P,luchuensis Mayr.) (Mamiya 1983).

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Monochamus in Exported Wood

For 200 years, massive quantities of NorthAmerican raw softwood products, including dunnage,logs, poles, wood chips, lumber, and other products,have been shipped to Europe and other countries.During these 200 years, the quantity and quality ofthese exported products have increased significantly.Over the last 12 years, Canada and the United Stateshave shipped nearly 5 million tons of softwood chipsrepresenting $160 million f.o.b. to Scandinavia. Itwould be naive to believe that some wood productsdid not harbor pine wood nematodes and the vectorlonghorn beetles at one time or another. The problemof pests in wood and wood products is not of recentoccurrence, only our perception of it.

Numerous reports exist of the interception oflonghorn beetles from pine wood pallets and crates(dunnage). According to Holdeman (1980) livespecimens of M. notatus, a species native to theNortheastern United States, emerged from pallets inCalifornia that had originated in West Virginia. Healso found records of a Monochamus species beingrecovered from dunnage aboard Japanese cargoships docked in San Francisco Bay. From 1985 to1987, longhorn beetles have been found associatedwith dunnage for commodities (manhole covers,granite, marble or tiles) imported into the UnitedStates from China, Spain, and Italy (USDA-APHIS1985-87). Longhorn beetles have been interceptedat New Zealand ports on many occasions (NewZealand Research Institute 1984).

The Scandinavian embargo includes timber cutfrom softwood trees. Canada reports that its gradedlumber is free of pine wood nematode-infestedlonghorn beetles (Hopper 1987). This aspect of theproblem has not been investigated in the UnitedStates, but there is no reason to believe that air-driedlumber represents a problem. The efficient loggingmanagement practices, quality controls, and inspec-tion and grading rules utilized in the United Statesshould preclude contamination by Monochamus Spp.

The rationale for the embargo on kiln-dried lumberby some countries is not consistent with the availablescientific knowledge on the organism. Commercialkiln drying of lumber is effective in killing all stagesof insects in wood, including Monochamus spp.(Ostaff and Cech 1978). Dwinell [In press] has foundthat B. xylophilus is eradicated from sawed lumberby kiln drying. Nematode mortality was attributed tohigh wood temperature (60 “C), not to moisture lossfrom the wood. One hour at 71 “C in a kiln was sufficientto eliminate nematodes from 2 by 4’s sawed from B.xy/ophilus-infested southern pine logs.

Infestation of Pine Chips:Risks and Management

The infestation of pine chips is what precipitatedthe bans by the Nordic countries. Dwinell (1986) hasstudied the ecology of the pine wood nematode insouthern pine chip piles and determined that theoptimum temperature for the reproduction of 8.xy/ophi/us in pine chips was 35” C. Mamiya (1983)reports that the nematodes will not reproduce atover 33” C on a mesophilic fungus in culture. Inwood chips, the nematode reproduces on mesophilicand thermo-tolerant fungi that invade the wood.

Dwinell (1987a) also studied the incidence of thepine wood nematode in southern pine chip pilesfrom (1) input onto the chip pile, (2) output from chippile to ship, and (3) discharge of chips in Sweden.Bursephelenchus xylophilus was found in chips beingdelivered to the terminal. Samples taken when theships were being loaded revealed that the populationof the nematode either declined or remained un-changed in the piled chips. Discharge samplesindicated, however, that the nematode populationincreased significantly during the trans-Atlanticvoyage. Distribution of nematodes in the holds couldbe related to the temperature of chips during transit.Maximum population levels occurred when thetemperature was around 35 “C.

Because of the deterioration of pulpwood chipsin outdoor storage, wood chip piles are very complexecosystems. The development of micro-organisms inthe chip piles is governed mainly by temperature.The interior of a pile of fresh wood chips rapidlyrises to 60 ‘C. Wiihin a few days, the living sapwoodcells die and there is a 50-percent loss in monoter-penes (Bergman 1985). After 3 days, piled freshchips of southern pine no longer attract adult pinesawyers (Cade 1987). Furthermore, the basic biologi-cal requirements of pine sawyers (Hellrigl 1971; Webb1909) cannot be met by wood chips. The risk of thenematode being vectored from wood chips appearsto be extremely remote.

After assessing the life history of the pine woodnematode and its complex association withlonghorned beetles of the genus Monocharms, NorthAmerican authorities agreed that the risk associatedwith importing wood chips and lumber into Scandinav-ia is virtually nonexistent, Scientists from the Nordiccountries, however, suggested there was a risk dueto chance transmission of the nematode to theScandinavian forests through casual visits of insectsto wood chip piles awaiting processing or the migrationof the nematode through the soil into adjacent foresttrees (Magnusson 1986).

9

In North America, nematodes have been foundin association with several insects, other than speciesof Monochamus emerging from nematode-infestedwood (Link and others 1983; Wingfield and Blanchette1983). For example, Linit and others (1983) found 3out of a total of 40 adult pales weevils (Hylobiuspales Herbat) from Scotch pine had a mean of 10 8.xy/ophi/us per adult weevil, Other studies, in Floridaon slash pine (Luui and Tarjan 1982) and in Minnesotaon Austrian pine (Wingfield and Blanchette 1983)examined 143 adult pales weevils without findingpine wood nematodes in any of them. Monochamusspp. are considered to be the only efficient vectorsof the pine wood nematode (Kobayashi and others1984; Linit 1987; Mamiya 1983, 1984; Wingfield andBlanchette 1983).

In comparison with other nematodes, B. xylophilusis unusual because ft is a parasite of abovegroundparts of trees, is carried by an insect, and does notenter the soil (Wingfield and others 1984). Thesuggestion of possible soil transmission is based ona study by Kiyohara and Tokushige (1971). Whetherthey demonstrated soil transmission is debatable. Inan experiment that lacked comparable controls,Kiyohara and Tokushige (1971) dug out the stembase and root system of five pines, attached anematode-infested disk to the root system, andcovered it with soil. The trees subsequently died. Itis quite possible, however, that the roots werewounded by excavating them. In a greenhouse study,Halik and Bergdahl (1987) mixed pine woodnematode-infested wood chips into the soil aroundwounded roots of 5-year-old eastern white pineseedlings. Seven of 12 seedlings treated with infestedchips wilted. Unfortunately, they did not use unwound-ed root controls. Because of the probability ofnematode-infested wood being adjacent to a woundedroot, neither of these studies demonstrates soiltransmission. Mamiya and Shoji (1988) concludedthat disease transmission through soil is negligible.They reported that pine wood nematodes added tosoil died within 48 hours. In an unpublished study, I

(Dwinell) mulched seedlings with B. xy/ophi/us-infestedchips for 12 months. The nematode was not transmit-ted to Scotch pine roots through the soil. I alsosurveyed the soil immediately below and aroundchip piles contaminated with pine wood nematodesand failed to extract any. Research to date suggeststhat the risk of soil transmission is minimal.

To further minimize these risks, Davis and others(1987) tried shipboard fumigation to kill nematodes.In 1986, a shipment of wood chips to Sweden wasexperimentally fumigated with phosphine (PH3. Thefumigation treatment was quite successful in eliminat-ing nematodes from wood chips. Intransit fumigationwas envisioned as a short-term solution to the problemthat would allow trade to continue until further researchand evaluation of the problem had been accom-plished. The exporters cannot afford to close downtheir terminals indefinitely.

In conclusion, it has become increasingly evidentsince 1983 that the pine wood nematode is mainly asecondary associate of conifers native to NorthAmerica and that the most common mode of transmis-sion is during oviposition of the Monochamus vector.Whether B. xylophilus is a primary pathogen ofstressed exotic pines is still open to question. In lightof our current knowledge about the biology of thepine wood nematode, European and other countriesmight want to reconsider their ban on U.S. andCanadian softwood forest products.

Acknowledgment

This report was prepared at the request of theStudy Group on Forest Insects and Diseases, NorthAmerican Forestry Commission, FAO. The authorsthank Jane Barrows-Broaddus, R.A. Blanchette, W.Friedman, A.M. Golden, R.A. Malek, and M.J. Linit forcritically reviewing the initial draft of the manuscript.

Mention of tradenames and companies issolely to identify experimental materialsand does not constitute endorsement bythe U.S. Department of Agriculture, nordoes it imply approval of a product to theexclusion of others that may also besuitable.

10

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Dwinell, L.D.; Nickle, W.R.

1989. An overview of the pine wood nematode ban in North America.Gen. Tech. Rep. SE-55 Asheville, NC: U.S. Department of Agriculture,Forest Service, Southeastern Forest Experiment Station. 13 pp.

The history, ecology, and biology of the Bursaphelenchus-Monochamuscomplex in North America are reviewed. Since the nematode is seldoma primary pathogen in North America, distribution there cannot beequated with the distribution of the pine wilt disease.

Keywords: Bursaphelenchus xyiophilus, Bursaphelenchus mucronatus,Pinus, embargo, softwood products, Monochamus, pine wilt disease.

Dwinell, L.D.; Nickle, WA.

1989. An overview of the pine wood nematode ban in North America.Gen. Tech, Rep. SE-55. Asheville, NC: U.S. Department of Agriculture,Forest Service, Southeastern Forest Experiment Station, 13 pp.

The history, ecology, and biology of the Bursaphelenchus-Monochamuscomplex in North America are reviewed. Since the nematode is seldoma primary pathogen in North America, distribution there cannot beequated with the distribution of the pine wilt disease.

Keywords: Bursaphelenchus xylophilus, Bursaphelenchus mucronatus,Pinus, embargo, softwood products, Monochamus, pine wjlt disease.

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