Bulletin OEPP/EPPO Bulletin 18, 353-363 (1988)

A survey for Bursaphelenchus spp. in pine forests in Norway

by D. G. McNAMARA* and M. ST0EN Norwegian Plant Protection Institute, 1432 h N L H (Norway)

Wood samples from pine trees were taken from 429 sites throughout Norway. The samples were selected as being either from ( I ) healthy trees, (2) trees suffering from stress, either physical or pathological or (3) dead trees. Nematodes were recovered from 39% of samples, most from dead wood and least from healthy trees. Species of Bursaphelenchus were recovered from 12% of dead trees and 5% of stressed trees, but were never found in healthy wood. B. mucronatus was found at just one site and in this sample it was associated with Monocharnus sutor, only one of two sites at which the beetle was detected. Based on the information gained from the survey and from other sources, an assessment is made of the risk of introduction ofB. xylophilus from outside Europe on imported wood and its survival, spread and disease potential in European forests.

Introduction

In 1984 a consignment of wood chips being transported from the United States to Finland was found to contain the pine wood nematode, Bursuphelenchus xylophilus (Steiner & Buhrer) and, as a result, a ban was placed by Finland on the import of all untreated coniferous wood products from those parts of the world where B. xylophilus occurred (Rautapaa, 1986). Similar bans were later imposed by Norway and Sweden when nematode-infested wood chips were intercepted en route from North America. The phytosanitary authorities in the Nordic countries were aware of the immense damage to the forests of Japan caused by this nematode, apparently introduced there from North America at the turn of the century (Mamiya, 1984). They considered that their heavily forested countries were most at risk from the introduction of this pest, particularly as the species of pine predominantly grown, Pinus sylvestris, had been shown to be one of the most susceptible to the nematode (Kondo et ul., 1982; Malek & Appleby, 1984).

A research programme was begun in Norway to try to assess the risk of the pine wood nematode to Norwegian forests: whether it could be introduced, could survive, spread or be pathogenic to native tree species. However, as no previous research had been performed on the nematode fauna of the aerial parts of the forest trees in this region, it was not known whether B. xylophilus might already be present in Norway, either as an indigenous species or a recent introduction with wood imports. Information on this point was considered essential before any meaningful risk assessment could be made, and therefore, the present survey was initiated to examine the nematode fauna of pine forests with particular reference to the genus Bursuphelen- chus.

As B. xylophilus seems to be so intimately connected with species of Monochumus in other parts of the world (Mamiya & Enda, 1972; Wingfield & Blanchette, 1983), it was considered essential to gain information on the distribution and frequency of representatives of the genus in Norway. Three species have previously been recorded in the country, M . galloprovincialis (Ol.), M . sutor L. and M . urossoui Fisch. (= rosemiilleri), of which the second named was the most common (Anon., 1960).

This paper presents the results of the survey and also an assessment of the risk to Norway in particular, but also with relevance to other European countries, of the introduction, spread and disease potential of B. xylophilus.

* Present address: EPPO, 1 rue Le NBtre, 75016 Paris (France).

353

3 54 D. G. McNamara and M . S t ~ e n

Materials and methods

Choice of sampling sites

As one of the main aims of the survey was to determine whether B. xyfophilus may have been introduced into Norway with recent wood imports, many samples were taken around the Oslo Fjord area and, especially, near the factory ports of Halden and Tofte. It was known that wood had been imported from North America to these sites.

Other sampling sites throughout the country were chosen so as to lie in areas of high pine concentration, i.e. Osterdalen, Gutbrandsdalen, Valdres, Numedal and Telemark. Apart from these considerations, samples were collected from as many sites in Norway as possible so as to give a wide distribution of points.

Types of samples

Samples were taken predominantly from trees of P. sylvestris and only occasionally from Picea abies. From each site, if it were possible, three basic types of wood sample were collected: (1) healthy trees; (2) trees whose foliage colour indicated that they were suffering from some form of stress, either mechanical (e.g. wind felling or breakage, root damage by drainage operations), environmental (e.g. frost, drought, water-logging), pathological (diseases or pests) o r of unknown cause; (3) dead wood of recent origin, within approximately 2 years. Each sample came from either one tree or from several trees within a radius of about 25 m.

Samples were taken from an area of forest of approximately 100 ha which was examined on foot during the course of a working day, or within an area of less than 1 ha where trees of a distinctive health status were observed; the latter type of sampling area was often chosen from a passing car.

From standing trees, major branches were cut close to the trunk with an extendible pruning saw and lengths of 15-20 cm were taken. If the sample tree was lying or if it was possible to fell a tree, discs were sawn from the trunk at several heights or chips of wood were taken with an axe.

Extraction of nematodes

Samples were stored in polythene bags a t room temperature for several days before extraction. All bark was then removed from the wood. Branch samples were cut into discs of about 5 mm thickness with a coarse-toothed mechanical saw. It was found that such a coarse-toothed saw generated little heat during cutting. Samples taken as trunk discs or axe chips were either similarly sawn or broken into smaller pieces. The wood pieces were then weighed and placed on a milk filter, supported on a plastic grid in a 30-cm-diameter Baermann funnel. After a t least 48 h the nematodes were collected and examined at x 25 magnification.

Nematodes of the genus Bursuphelenchus were mounted and examined by interference contrast microscopy at x 1000. Other nematodes were preserved in a solution of triethanola- mine/acetic acid/formaldehyde (TAF) (Southey, 1970) and stored in the Norwegian Plant Protection Institute for possible future examination.

Sampling for Monochamus

At each nematode-sampling site attempts were made to locate species of Monochumus, mostly by visual observation. Bark was removed from dying or dead trees to seek evidence of larval feeding, especially the characteristic tracks of chewed surface wood, the oval entry holes into the trunk made by older larvae or the circular exit holes made by the adults (Tragtirdh, 1929).

Survey for Bursaphelenchus in Norway 355

Suspect larvae were collected and bolts of timber were brought back to the laboratory. During the months of June, July and August, when M . sutor swarms in the Nordic countries (Bakke, 1961), piles of recently cut logs, left beside forest roads for later collection, were examined for adult beetles engaged in oviposition.

Fig. 1. Distribution of samples from Pinus sylvestris in Norway. Each point represents a LO-km square in which one or more samples were taken. Rtpartition des points d’echantillonnage de P. sylvestris en Norvege. Chaque point correspond a un carrt de 10 km dans lequel au moins un tchantillon a t t t prelevt.

356 D. G. McNamara and M . Stgen

Results

Nematodes

Throughout the country, 429 samples were taken, distributed as shown in Fig. 1, from healthy, stressed or dead trees (Table 1). Approximately 40% of the total number of samples contained nematodes of some sort but these mostly came from dead wood; only 18.4% of the healthy samples contained nematodes (Table 1). Most of the nematodes recovered were saprozoic species belonging to the order Rhabditida; second to those in frequency were Aphelenchida (mostly Aphelenchoides spp.) with occasional representatives of the Tylenchida (Neoditylenchus and Neotylenchus spp.). These nematodes were not identified exactly but were preserved in TAF.

Twenty-six samples contained species of Bursaphelenchus (Fig. 2). In most cases these nematodes probably belong to species new to science and it is intended that they should be described in a future publication. There appear to be at least two new species, morphologically closely related to B. bakeri Riihm. Although almost nothing is known about their life histories, it is most probable that they are transmitted by bark beetles and that they live as fungal feeders in dead wood (Riihm, 1956). These Bursaphelenchus spp. were never found in the wood of healthy trees and there is no evidence that they are pathogenic to pine.

From a sample taken from cut logs at Hanestad in 0sterdalen (Fig. 2), nematodes were found which were identified as B. mucronatus Mamiya & Enda.

B. mucronatus belongs to the same group of the genus Bursaphelenchus as B. xylophilus (Giblin & Kaya, 1983) and the two species are very similar, being identical in the major morphometric characters. The only distinct morphological difference is in the shape of the female tail. Mamiya & Kiyohara (1 972) described B. xylophilus (then named B. lignicolus) as having a tail which was smoothly rounded but occasionally with a short mucro, whereas B. mucronatus (Mamiya & Enda, 1979) was described as always having a long mucro. Later, a form with an intermediate tail shape was discovered in northern USA and it appeared that B. xylophilus occurred in two forms, the R-form (for ‘Round-tailed’ form) as in the original description and the M-form (‘mucronated-tailed’) which has a mucro but a more rounded tail than B. mucronatus (Wingfield et al., 1983).

Such differences seem a rather small base for separating species but the morphological differences have generally been associated with differences in pathogenicity (Mamiya & Enda, 1979); the R-form is the most pathogenic to Pinus spp., the M-form is less pathogenic and is often found in other genera of conifers, whereas B. mucronatus is apparently non-pathogenic (Wingfield et al., 1983).

Another small difference between the original descriptions of the two species, but one which is rather difficult to see and which has not been commented upon as much as the female tail shape, lies in the shape of the bursa of the male. B. mucronatus was described as having two small

Table 1. Nematodes recovered from pine samples of different types taken throughout Norway. Presence de ntmatodes dans des tchantillons de bois de pin provenant de sites repartis sur l’ensemble de la Norvtge.

Sample type Total With nematodes With Bursaphelenchus __.

Healthy 118 21 0 Stressed 157 43 8 Dead wood 154 106 18 Total 429 169 26

Survey for Bursuphelenchus in Norway 357

Fig. 2. Distribution of samples from Pznus syluestris in Norway from which species of Bursaphelenchus were recovered (cf. Fig. 1). The arrow marks the site at Hanestad at which B. mucronatus was found. Possible Monochamus larvae were also found at Hanestad and at the site marked by the open circle. Rkpartition des points d’echantillonnage de P. syluestris en Norvkge ou la presence de Bursuphelenchus spp. a CtL decelee (cf. fig. 1). B. mucronafus identifie i Hanestad (flkhe), ainsi que des larves de Monochumus (trouvees aussi au site indiqud par le cercle blanc).

projections on the terminal margin of the bursa (Mamiya & Enda, 1979), whereas B. xylophilus was said to have just a single point (Mamiya & Kiyohara, 1972). However, Baujard (1980) questioned if this was a consistent difference.

The morphological features of the nematode found at Hanestad point clearly to it being B. mucronatus; the rounded female tail with its long mucro is characteristic of the species and the male bursa plainly shows the two projections (Fig. 3) .

358 D. G. McNamara and M. St0en

Fig. 3. Tails of adults of Bursuphelenchus mucronatus from Hanestad. Above: male, showing the two points of the bursa (arrowed). Below: female. Queues d'adultes de B. rnucronatus provenant de Hanestad. En haut: mHie, avec bourse a deux pointes (fleche); en bas: femelle.

Survey for Bursuphelenchus in Norway 359

Monocharnus

At only two sites in this survey (Fig. 2) were insects found which could be species of Monochamus. The identification was based originally on larval characteristics; positive identification of M . sutor was performed only on emergence of adult beetles from bolts of timber, from one of the sites, stored in the laboratory. No adults emerged from wood collected at the other site. The specimens of B. mucronatus mentioned above were recovered from one of these samples, at Hanestad. No Bursaphelenchus species were found in the other sample, from Sjoa in Gudbrandsdalen. Except in these samples, no evidence was obtained for the presence of Monochamus at any of the sites, neither as wood damage on dead wood of recent origin or many years old, nor as ovipositing adults on fresh-cut logs.

Discussion

Discussion of results

A primary object of this survey was to determine if B. xylophilus was present in Norway, and the answer appears to be that it is not. Ofcourse, such an answer must be treated with caution, based as it is on the small proportion of samples compared to the actual number of pine trees in the country. However, every effort was made to obtain a representative aliquot by covering as much of the country as possible and by obtaining samples from the different types of pine forest which exist: the timber forests of Telemark, Gudbrandsdalen and Osterdalen, the marginal forests of high altitude or poor terrain, and the pine trees growing within predominantly spruce forests. Furthermore, by concentrating on stressed trees or dead wood it was felt that there was a greater chance of locating nematodes transmitted by beetles which utilize wood of this type. The fact that other species of Bursaphelenchus were commonly found gave confidence that B. xylophilus would also have been found had it occurred. The presence of the other Bursaphelenchus spp. also allowed sampling and extraction procedures to be tested and modified during the course of the study.

What can be stated with more confidence is that there is almost certainly no pine wilt disease in Norway. Much of the country was travelled during the course of the survey, always looking for those symptoms associated with pine wilt disease in other countries. Wherever such symptoms were seen it was generally possible to identify the cause as being of some other origin, most commonly mechanical damage, environmental, stress or other pathogens. Furthermore, if pine wilt disease had been the cause, the wood would have contained large numbers of nematodes (Mamiya, 1984), and this was obviously not the case.

Any conclusions concerning Monochamus, its association with Bursaphelenchus and its overall distribution in Norway must also be tentative, being based on a survey limited in extent and time span. However, the fact that B. mucronatus was found only where Monochamus was also found confirms the observations made in other countries (Mamiya, 1984) that this group of Bursaphelenchus is very closely dependent, ecologically, on species of Monochamus. The survey also showed that M . sutor has apparently become very rare in recent years; less than 50 years ago it was considered to be the most serious pest of cut timber in the Nordic countries (Tragirdh, 1940). Why this should have changed is difficult to say. Perhaps the standard of forest hygiene in Norway has improved to such an extent after the epidemic of Ips typographus during the previous decade (Bakke, 1983) that suitable oviposition sites are difficult for the beetle to find; or silvicultural practices have changed so that logs are now removed from the forest at a particularly vulnerable point in the beetle’s life history; or human activities have tipped the balance in favour of other beetles which compete directly with Monochamus. Whatever the reason, it also may have had the effect of limiting the distribution of B. mucronatus; it was found in only one sample out of 429. This find of the nematode was so far from the sea that it argues against the possibility of this species being introduced with imported timber.

D. G. McNamara and M. St~len

Global distribution

It has recently been predicted by Rutherford & Webster (1987) that future surveys reveal that B. xylophilus is distributed throughout the Northern Hemisphere, being found just as much in Eurasia as in North America, and that its potential for damage to pines is limited only by climate. Furthermore, it is suggested that susceptible Pinus spp. are limited to north of the July 20 "C isotherm by such a climate-related disease potential of the nematodes.

It could just as easily be argued that a precursor species to both B. xylophilus and B. mucronatus once had a distribution throughout the Northern Hemisphere but that, later, there was a separation (by the Bering Strait) into two species, B. xylophilus in North America (with its southern round-tailed form and its northern mucronated-tailed form) and B. mucronatus in Eurasia. Neither of these species damage the native species of their natural range. The situation is complicated only by an accidental introduction of the M-form of B. xylophilus into southern Japan and its subsequent spread northwards and to China. The status of the Bursaphelenchus species in France is unclear, being apparently closer in morphology to B. mucronatus but intermediate in pathogenicity between the two (De Guiran & Boulbria, 1986). It is either a native European B. mucronatus or perhaps an introduction from Canada, as indicated by its limited distribution around a west coast port, of the M-form of B. xylophilus.

The distribution of the nematodes in North America is quite well known (Robbins, 1982) and a continuing survey in Canada (Anon., 1986) is still producing data, but, so far it is only known that B. mucronatus occurs in Japan, China (Mamiya, 1987) and in unspecified parts of the USSR (as detected on imported timber into Finland) (A. Lahtinen, pers. comm.) The present survey is the first positive identification of B. mucronatus in the Nordic countries. Schauer-Blume (1987) reports the presence of a 'B. mucronatus-like' nematode in dead oak wood in the Federal Republic of Germany, but the illustrations of the adult tail shapes suggest that it is a different species from the Norwegian specimens. Surveys in Finland (Rautapaa, 1986), Sweden (C. Magnusson, pers. comm.), the Netherlands (Bongers, 1986) and Austria (Schmutzenhofer, 198 1) failed to detect it but these surveys were of a limited nature and, perhaps, a concentration on Monochamus spp. might reveal the presence of B. mucronatus.

Risk assessment

It is obviously undesirable that barriers to international trade should be maintained any longer than is absolutely necessary but, equally, such trade should be strictly regulated if there is a danger of introducing an agent from abroad which is likely to threaten a precious natural resource. The worst possible eventuality would be that wood chips containing B. xylophilus would be brought to northern Europe and that the nematodes would escape to the forests where they would survive the climatic conditions and be transmitted by native species of Monochamus to cause similar forest destruction to that observed in Japan.

To make a realistic assessment of whether the pine wood nematode could be a danger to the European forest industry, it is necessary to consider, in turn, the various possible stages of introduction, survival, spread, pathogenicity and epidemic potential of the nematode in relation to European conditions.

Magnusson (1986) attempted to evaluate the risks of introducing the nematode into Europe with wood chips. He considered the possibilities of either foreign species of Monochamus being introduced or of nematodes being transmitted from chip piles in Europe by means of native beetle (or other insect) species or through the soil. His general conclusion was that, although in each of these cases the risk was small, it was still a possibility which must be guarded against.

During the present survey it was observed that wood chips were used as mulch between the rows in a strawberry plantation surrounded by pine trees; the chips had been obtained from a factory which had, in the past, imported chips from abroad. On another occasion wood chips

Survey for Bursaphelenchus in Norway 361

were found in a forest, having apparently fallen from a vehicle collecting logs for transport to a similar factory. It is not suggested that in these cases the chips were of foreign origin, but the incidents illustrate how easily infected chips could reach the forest. If an infected chip should fall on a cut tree stump or on a fallen log, the nematodes could thereby enter the natural ecosystem of the forest and soon come into contact with potential vectors.

The danger of transporting insect vectors with round wood is obviously much greater. Logs are most commonly transported after a debarking procedure which would effectively eliminate the bark beetles, but not species of Monochamus which may already be deep in the wood before debarking. Furthermore, such procedures are not always perfect (Venn, 1986) and there is the possibility that bore holes could remain undetected under remnants of bark during phytosani- tary inspection. Foreign species of Monochamus may not be capable of surviving for long under Northern European climatic conditions, but perhaps long enough to transmit nematodes during feeding or oviposition attempts.

Of course, sawn lumber does not present so great a risk of beetle introduction, although adult Monochamus have occasionally been observed coming out of pine panelling within houses in Norway (A. Bakke, pers. comm.) and there is a record of a foreign species of Monochamus emerging from a piece of pine furniture in Great Britain 15 years after manufacture (Hickin & Edwards, 1974). Nematodes may still be present in such lumber and the sawdust produced during further use of the wood could present similar risks in transportation by humans, as outlined for chips.

It is highly likely that B. xylophilus could survive in northern Europe, as evidenced by its distribution in Canada (Anon., 1986) and it is also likely that it could find a vector there. The fact that B. mucronatus was only found in a sample also containing M . sutor is a strong indication that the latter is the vector of that species of nematode, and presumably could also transmit B. xylophilus. Furthermore, the apparent rarity of the beetle in Norway should not be taken as a cause for comfort until the cause of its rarity is known; one can recall that Monochamus was also rare in Japan before the disease began to spread (Mamiya, 1984). Other beetle species, especially genera of the Cerambycidae, could transmit B. xylophilus in a non-specific manner (perhaps only during oviposition) until the nematode came into contact with its specific vector.

Pine wilt disease has so far occurred predominantly in areas of high temperatures. Magnusson (1 986) in his risk assessment pointed out that trees in northern Europe are very often subjected to a range of stress factors other than high temperatures. Bolla (pers. comm.) has demonstrated that pine wilt disease incidence can be increased by subjecting plants to stresses induced by heavy metals and by acid precipitation. As it is known that many European trees are subjected to atmospheric pollution of this kind it is conceivable that they could succumb to a nematode attack.

Conclusion

To summarize the risk assessment in just a few words it can be said that, until more information becomes available, the survival and the spread of the pine wood nematode in northern Europe are both quite possible, if the nematode should be first introduced, and that pine wilt disease would also be a probable event, especially in the case of trees already suffering some other form of stress. The chances of introduction seem small but this would be most likely to occur as a result of careless human transport of chips. The risk may be small but the price of introduction could be very large indeed. An epidemic, such as is occurring in Japan, would, of course, be disastrous for countries with extensive forest industries, but even if the disease could not develop in northern Europe, the very presence of the nematode in these countries could lead to a restriction on their wood exports to countries more likely, for climatic reasons, to be susceptible.

362

Acknowledgements

The authors are grateful to NISK, de Kongelige Landbruksdepartement and NLVF for financial support. We thank those colleagues who helped in collecting samples, in particular the members of Programmet for Skogskader. We recognise the invaluable technical assistance of Solveig Haukeland, Esther Markussen and Bonsak Hammer&

D. G . McNamara and M . Stt~en

Recherche de Bursaphelenchus spp. dans les forQts norvegiennes de pin

Des echantillons de bois ont &ti. preleves sur pin a 429 sites repartis dans I’ensemble de la Norvkge, sur des arbres soit sains, soit visiblement stresses (physiquement ou pathologique- ment), soit morts. Sur l’ensemble des echantillons, 39% (provenant surtout d’arbres morts) contenaient des nematodes. La presence de Bursaphelenchus spp. a ete constatke dans 12% des arbres morts et dans 5 % des arbres stresses, alors que ces nematodes ttaient systematiquement absents des arbres sains. B. mucronatus a ttk trouve a un seul site, associe a Monochamus sutor qui n’a d’ailleurs CtC trouve qu’i un seul autre site. Les resultats de cette prospection et d’autres donntes ont servi a une evaluation du risque d’introduction de B. xylophilus sur bois import6 en Europe, ainsi que de son potentiel de survie, de dissemination et de pathogenbe dans les forits europtennes.

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