Root parasitic nematodes in nursery plants imported to Finland in 1980.

Injurious nematodes were found in 201 of the investigated 670 plant stocks of 42 imported consignments. Infections by quarantine nematodes appeared in 100 stocks of 26 consignments, 15 thereof including 3 or more infected plant stocks each. Root knot nematode, Meloidogyne spp., appeared in 81 stocks, i.e. 12 % of the investigated material. The infections were found in 40plant species, relatively often in barberry, Herberts sp., and in peony, Paeonia sp.. Among garden roses, 26 out of 167 stocks investigated were infected by root knot nematodes. Root lesion nematode, Pratylenchus penetrans (Cobb) Chitwood & Oteifa, of P. convallariae Seinhorst was found in 28 plant stocks, i.e. 4 % of the investigated material. Several Pratylenchus-'mfecled stocks were found among roses, raspberry and barberry. Potato rot nematode, Ditylenchus destructor Thorne, was found in one rose stock and related D. myceliophagus J. B. Goodey in 12 stocks of various plants. Several ectoparasitic species were found in very low numbers. Virus vectors, Trichodorus primitivus (de Man) Micoletzky and T. viruliferus Hooper, were detected in a total of four stocks, but too few for virus transmission tests. The transmissability of the detected nematodes was discussed, and the risks of introduction of nematode pests to the country was re-assessed.


Introduction
Dispersal of nematode pests in the international market of plant material has repeatedly been reported (Bingefors 1967, Braach 1978, Esser 1978. In the 1950's the introduction of the stem nematode, Ditylenchus dipsad (Kuhn) Filipjev, and the sugarbeet nematode Heterodera schachtii Schmidt was associated with the import of their host plants to Finland (Roivainen 1961, Roivainen et ai. 1962). Later, a few cases of introduced root knot nematodes, Meloidogyne sp., have appeared in greenhouse cultivations. In 1976-80, the import of nursery plants, especially roses, was prohibited on the basis of local phytosanitary regulations because of root knot nematodes (Anon. 1976-80).
In 1975-80, plant propagation material for Finnish horticultural nurseries was imported mainly from Central Europe, particularly from the Netherlands, and occasionally from non-European countries (Anon. 1976-80).
In the few surveys published on the growing areas of European nurseries, certain root parasitic nematodes, including Meloidogyne and Pratylenchus species occured commonly (Nolte and Dieter 1957, Sonderhousen et al. 1968, Kozlowska and Wasilewska 1972, Saly 1979, Gotten and Roberts 1981.
The objective of this survey on plant material imported to Finland in 1980 is to reveal the potential sources of nematode infections risky for nursery cultivation in the field as well as in greenhouses.

Samples
Root samples were taken in April 1980 arbitrarily from the imported plant material by the quarantine officers performing routine plant inspection. The number of samples taken was 670, and each sample represented a uniform stock of imported plants. Samples were taken from 42 consignments, each sent by one exporter and including a minimum of 10 plant stocks. The consignments came from European countries: 17 from the Netherlands, 15 from Denmark, 7 from West Germany, 1 from Belgium, Sweden and United Kingdom, each. (The total distribution of consignments from these countries in 1976-80 was 65°7o, 18 %, 6°7o, 4°7o, 5 % and 2°/o, respectively.) The size of the samples varied between 20-200 g, depending on the structure of the root system, big samples taken from roots with large diameter. The samples were transported in closed plastic bags.

Extraction and identification
In the laboratory of the Department of Agricultural and Forest Zoology, University of Helsinki, the uncleaned roots were cut or chopped into pieces of less than 0.5 cm in size and a subsample of 10 g was processed by the centrifugal flotation method (Cavevess and Jensen 1955) and another subsample of 10 g on a mistifier apparatus (Hooper 1970 a) for five days to extract the nematodes. The nematodes were thereafter fixed in a mixture of formalin, triethanolamine and water (T.A.F.) (Hooper 1970 b). The total number of nematodes and the number of nematodes of the genera Ditylenchus spp., Meloidogyne spp., the spiral nematodes {Helicotylenchus spp., Rotylenchus spp.), Tylenchorhynchus spp., the trichodorid nematodes and the longidorid nematodes were counted. The identifications were done from subsamples mounted in glycerol by the Seinhorst slow method (Hooper 1970 b). Special attention was paid to species mentioned in the plant quarantine regulations issued in Finland. A sample was defined as infected if any of the above nematodes could be detected by either of the two extraction methods.

Frequency of infections
Nematodes belonging to the genera Ditylenchus, Meloidogyne, Pratylenchus, Helicotylenchus, Rotylenchus, Tylenchorhynchus and Trichodorus were found in 201 of the 670 investigated root stocks. The number of infections specified in the quarantine regulations was 115 in 100 stocks. The occurrence of infections in the most commonly imported plants is presented in Table 1. The infected plant stocks were distributedby consignments as follows: all plant stocks in a consignment free from any quarantine infections 16, one stock infected 4, two stocks infected 7, and 3 or more stocks infected 15 consignments (mean 3.8). (The consignments consisted a minimum of 10 plant stocks.)

Potato rot nematode
The plant parasitic Ditylenchus species was rarely encountered ( Table 1). The only D.
destructor infection was found in rose stock (cv. Europaena) also infected by Meloidogyne spp.. No visible symptoms were seen in the infected roots. The other Ditylenchus species was D. myceliophagus J. B. Goodey which was found in 12 root stocks of the following plants: Ajuga reptans L.
L. Clematis x jack-Prunus padus L. manii T. Moore Rosa L. sp. Picea abies L. The highest number of juveniles appeared in a stock of Phlox paniculata (150 juveniles / 10 g roots). There were no symptoms in these roots. Among roses, the highest number of infections and also the highest number of nematodes per sample were found in garden roses but also 3 out of 10 stocks of multifloral roses for house plants were infected.

Root lesion nematodes
Of the two phytosanitarily important Pratylenchus species, P. penetrans occured more commonly (Table 1), and the infections of P. penetrans were slightly stronger than those of P. convallariae. All the infections were weak, the maximum number of adults and juveniles in the roots being 50 P. penetrans and 35 P.

Discussion
The high frequency of Meloidogyne infections was expected on the basis of the superior international dissemination of these nematodes (Sasser 1977). Larvae of Meloidogyne spp. where, however, rare in the Danish nurseries and rose fields (Sonderhousen et al. 1968) and equally infrequent further south (Wolny 1980, Kozlowska and Wasilewska 1972). The fairly high frequency of Meloidogyne spp. larvae in roots of this survey may have several explanations. Either the imported plant material originated from particularly highly infected areas or even from third countries, or the material was infected during preparation for exports or during transportation.
The inadequate capacity of transferred root knot nematodes to adapt to new situations (Sasser 1977) must be the reason why Meloidogyne infections have not been more frequent in local nurseries. In greenhouses, many species of the root knot nematodes can be expected quickly to build up injurious populations. It is therefore of major importance that attention be paid to the quality of the material. In open fields the maximum accumulated temperature in southern Finland is in most years double the temperature needed for larval development of M. hapla (Vrain et al. 1978).
Survival of infective populations of M. hapla in comparable conditions has been shown (Johnson and Potter 1980). The great strain specific differences in temperature thresholds for survival demonstrated with M. javanica by Daulton and Nusbaum (1961) and the ability of Sayre's M. hapla population to tolerate freezing temperatures (Sayre 1964) are of special concern.
The Pratylenchus species described above riods without a host plant (Seinhorst and have, previously, been found in Finland (Sarakoski 1978). P. penetrans has caused injuries in greenhouse carnations, young apple trees, Crataegus sp. and onions (Anon. 1963 -64, Sarakoski 1978). The low frequency of Pratylenchus spp. in the detected roots, in contrast to the high frequency of these nematodes in the European nurseries (Sonderhousen et al. 1968), might be due to the nematodes' mobility during harvesting or storage of the plants for import. P. penetrans has shown properties which make it transportable (Wyss 1970), and Wolny (1980) found quite a number of root lesion nematodes in the roots of nursery plants grown in infested soil. After all, even a weakly disseminated population might become important because of the relatively high infectivity of Pratylenchus species at low temperatures (Ferris 1970, Kimpinski andWillis 1981) and because of their interactions with pathogenic fungi.
The ectoparasitic nematode species found here were mostly the same as found by Wolny (1980). Many of them are capable of adaptation, enabling survival during transportation in roots which should be free from any loose soil. D. myceliophagus forms 'curds', aggregates of a cryptobiotic stage (Cairns 1953, Perry 1977. D. destructor which is devoid of any inactive stage can, on the other hand, survive on fungal hyphae. The Paratylenchus species and T. claytoni are at a certain stage able to stay inactive and desiccated even for years (Mcglohon et al. 1962,Brzeski 1976). T. dubius has been mentioned cabable of being spread by wind (Simons 1973), and some unidentified Helicotylenchus nematodes were found cabable of the same (Orr and Newton 1971). R. robustus survives long pe-Keniasu 1969) and has been found fairly drought tolerant (Wyss 1970). The nematodes most sensitive to desiccation and to all disturbances are the trichodorides (Wyss 1970).
T. viruliferus is, however, known to shield itself by burrowing into cracks it has produced in the roots (Pitcher and Mcnamara 1970).
No such behaviour has been reported about T. primitivus.
The introduction of the above mentioned and other new ectoparasitic species is highly probable, but establishment of injurious populations of the species is unlikely if the infections remain as weak as here described. However, severe infestations of the potato rot nematode, D. destructor, has been reported in southern Sweden (Andersson 1967), and the nematode has a great number of hosts among Finnish plants and many universally common fungal hosts (Faulkner and Darling 1961). The populations of T. dubius are known to increase at 10°C (Malek 1980). R. robustus was injurious in the Scottish forest nureseries and it has been shown to start feeding at a temperature as low as O.5°C (Boag 1980), but its development is very slow (Boag 1982).