United States Department of An Overview of the Agriculture Forest Service Pine Wood Nematode Ban . in North America Southeastern Forest L.D. Dwinell Experiment Station General Technical W.R. Nickle Report SE-55 North American Forestry Commission Publication No. 2 May 1989 Southeastern Forest Experiment Station F?O. Box 2680 Asheville, North Carolina 28802 An Overview of the Pine Wood Nematode Ban in North America L. D. Dwinell, Principal Research Plant Pathologist Southeastern Forest Experiment Station Forestry Sciences Laboratory Athens, Georgia W. R. Nickle, Research Nematologist USDA Agricultural Research Service Systematic Botany, Mycology, and Nematology Lab Beltsville, Maryland ABSTRACT These events resulted in a rapid exchange of The history, ecology, and biology of the Bursaphelenchus- information between the countries concerned. Fact- Monochamus complex in North America are reviewed. The pine finding teams from Finland, Norway, and Sweden wood nematode (B. xylophius) is a secondary associate of native visited the United States and Canada. The ban has conifers and the most common mode of transmission is during been costly to the forest industries in North America. oviposition of the Monochamus vector. The pine wood nematode Understandably, however, the importing countries is a primaty pathogen of exotic pines, however. Primary and secondary transmission of B. xylophilus are described. Since the are concerned about the health of their forests and nematode is seldom a primary pathogen in North America, do not want to experience a pine wilt disease epidemic distribution there cannot be equated with the distribution of the such as has occurred in Japan (Mamiya 1988, 1984). pine witl disease. Recent research on the incidence, control, and They must evaluate the magnitude of the problem in risks of the pine wood nematode and its vectors in exported softwood Japan, the problem on Scotch pine in the Midwestern products is reviewed. United States, and the possible threat to the forests Keywords: Bursaphelenchus xylophilus, Bursaphelenchus mucrona- of Nordic and other European countries. Recent tus, Pinus, embargo, softwood products, Monochamus, pine wilt discussions with European scientists and government disease. officials suggest that the current status of the pine wilt disease in North America is not fully understood there. For example, the opinion has been expressed that some exported pine chips are from trees killed by a pine wilt epidemic in North America. One of the Embargo main arguments put forth by Rautapaa (1986) of Finland was that ‘the nematode has caused significant Recent events have focused new attention on economic damage to pines in USA and in Japan.’ the status of the pine wood nematode, Bursaphe- EPPO (1986) stated that the pine wood nematode is lenchus xy/ophi/us (Steiner & Buhrer) Nickle (= B. associated with tree dieback in Canada. In fact, pine lignicolus Mamiya & Kiyohara), in North America. In wood nematodes are seldom, if ever, the primary 1984, pine chips headed for Finland from the United cause of mortality of conifers in the forests of North States (fig. 1) and Canada were found to be infested America. by pine wood nematodes (Rautapaa 1986). Since this nematode was considered to be the causal New Perspectives on Past Research agent of pine wilt disease (Mamiya 1988, 1984) Finland in 1985 banned importation of conifer chips Research on a pest such as the pine wood and timber cut from softwood trees grown in areas nematode is a dynamic process. Each new discovery of the world in which the pine wood nematode occurs provides fresh insight, which sometimes changes (Rautapaa 1986). The other Scandinavian countries one’s perceptions of the pest and the disease it followed suit. In July 1985, the European Plant causes, and requires a critical reevaluation of the Protection Organization (EPPO) recommended that previous literature. Scientists in a network that actively Europe as a whole ban softwood products except exchanges information frequently recognize the subtle kiln-dried lumber from countries known to have B. changes in direction before the scientific community xy/ophi/us (Smith 1985). at large. Unfortunately, the significance of such discoveries is not always fully appreciated. This report examines some new observations on species similar to B. xy/ophi/us, may be the aboriginal the pine wilt disease complex. It places the current inhabitant of M. akernatus in Japan (Mamiya 1988; status of the pine wood nematode and the pine wilt Mamiya and Enda 1979). disease in North America into perspective. ‘Perspec- tives; as Van Gundy (1986) noted, ‘are the way we In the United States, dauerlarvae of B. xy/ophi/us see and interpret things based on our own experience have been recovered from adult beetles of M. and individual philosophies.” carolinensis Oliver, M. scutellatus Say, M. titilkor Fabricus, M. muraror LeConte, M. scutellatus orego- nensis (LeConte), and M. nofafus Drury (Holdeman &&Q Initial Reaction to Rediscovery of Pine 1980; Linit and others 1988;I(Uickle and others 1980; 1 f@y- Wood Nematode in North America Tarjan and others 1980; Wingfield and Blanchette 1988. A possible strain of 8. xy/ophi/us in which the The pine wood nematode (as B. lignicolus) was adult females have mucronate tails similar to those first reported from North America in 1979. It was of B. mucronafus is phoretic on M. marmorator and found on dead Austrian (Pinus nigra Arnold) and M. scurellafus (Wingfield and Blanchette 1988). Scotch (P. sylvesfris L.) pines in Missouri (Dropkin and Foudin 1979), and was thought to have been In Canada, 14 potential insect vectors of the introduced from Japan. The initial reaction by the pine wood nematode are known to be present scientific community, reflected in the literature of the (Garland 1985). These include six species of longhorn time, was ‘We’ve been invaded!” (Hoideman 1980). beetles: M. carolinensis, M. marmorafor, M. mutator, In 1981 B. lignicolus, the Japanese nematode, was M. obtusus Casey, M. scutellafus, and M. titillator. synonymized with B. xy/ophi/us (Nickle and others Bursaphelenchus xy/ophi/us was first reported in 1981), a species known to occur in North America. Canada in 1988 (Knowles and others 1988). Earlier, Nickle (1970) had transferred Aphelenchoides xylophilus Steiner & Buhrer to Bursaphelenchus. Research in Mexico on longhorn beetles has Aphelenchoides xylophilus had been found in associa- been limited. Monochamus nofafus has been reported tion with fungi in downed timber (Steiner and Buhrer on Pinus spp. and Abies spp. in Mexico State, and 1984). Although the pine wood nematode has been M. rubigineus Bates (= M. clamafor rubigineus (Bates) known to be in North America for at least 60 years Linsley & Chemsak) have been found on P. pa&/a in and is probably a native species, research in the Hidalgo State (Samaro 1987). Reportedly, M. clamator United States has continued to emphasize pathogene- rubigineus has a range from southeastern Arizona to sis. In a thorough evaluation of the problem, Holdeman Honduras, and the host plants include P. leiophylla (1980) concluded that the pine wood nematode was Schiede & Deppe and P. ponderosa Dougl. ex Laws. not a threat to conifers in California. Some landmarks (Linsley and Chemsak 1984). Samano (1987) howev- in the history of research on the pine wood nematode er, believes that several other species of Monochamus, are outlined in table 1. including known vectors of the pine wood nematode, occur in Mexico. Although B. xylophilus has not been Relationship of Bursaphelenchus With reported in Mexico, its existence there is highly Monochamus probable. Most of the 49 described species of Bursaphe- The biologies of the Asian, North American, and lenchus have a phoretic relationphip with insects, Euro-Siberian Monochamus species are similar. especially bark beetles and wood borers, $nd all are ,f, , Species differ in geographical distributions, host mycophagous (Massey 1974; Rijhm 195 . The pine ‘I’ ti plants, oviposition site preferences (location on trunk, wood nematode and other closely relat zspecies of *etc )I 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). the genus Monochamk. These beetles are saprophyt- ic wood borers in the larval stage (Hellrigl 1971; Linit The adult sawyers are attracted to recently dead 1987; Webb 1909). or dying trees and freshly felled timber (including logs) for breeding. The cause of the conifer’s mortality In Japan, China, and Taiwan, M. alternatus Hope is not particularly significant. In the United States, for is the primary vector of B. xy/ophi/us (Mamiya 1987; example, sawyers breed in pines killed by other Mamiya and Enda 1972). Monochamus nifens Bates insects such as the southern pine beetle (Dendroc- & M. saltuarius Gebler are also considered to be tonus frontalis Zimm.) (Coulson and others 1976; vectors in Japan (Kobayashi and others 1984). Dwinell 1988) or the engraver beetle (Ips calligraphus Bursaphelenchus mucronarus Mamiya & Enda, a Germ.) (Miller 1984), by root rot and drought (Dwinell Table 1. -Some landmarks in the history of pine wood nematode research Year Event Reference 1909 Biology of Monochamus ririlaror described Webb 1909 1929 @he/enchoides xy/ophi/us found in association with fungi in timber Steiner and Buhrer 1934 1969 Bursaphelenchus sp. found in wood of dead pine trees in Japan Tokushige and Kiyohara 1969 1970 Aphelenchoides xy/ophilus transferred to Bursaphelenchus Nickle 1970 1971 Pathogenicity of Bursaphelenchus sp. demonstrated by 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 Monochamus alrernarus reported (maturation feeding) Mamiya and Enda 1972 1979 Bursaphelenchus mucronarus is described Mamiya and Enda 1979 Pine wilt disease reportedly found in the United States Dropkin and Foudin 1979 1981 Bursaphelenchus lignicolus placed as a synonym of B.