2 Maataloustieteellinen Aikakauskirja Vol. 57: 155—162, 1985 Root parasitic nematodes in nursery plants imported to Finland in 1980 SIRPA KURPPA Agricultural Research Centre, Department of Pest Investigation, 31600 Jokioinen, Finland Abstract. 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 investi- gated material. The infections were found in 40plant species, relatively often in barberry, Her- berts 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. conval- lariae 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) Mi- coletzky 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 introduc- tion of nematode pests to the country was re-assessed. Introduction Dispersal of nematode pests in the interna- tional market of plant material has repeated- ly been reported (Bingefors 1967, Braach 1978, Esser 1978). In the 1950’s the introduc- tion of the stem nematode, Ditylenchus dip- sad (Kuhn) Filipjev, and the sugarbeet nema- tode Heterodera schachtii Schmidt was asso- ciated 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 ap- peared in greenhouse cultivations. In 1976—80, the import of nursery plants, espe- cially roses, was prohibited on the basis of lo- cal phytosanitary regulations because of root knot nematodes (Anon. 1976—80). In the Finnish quarantine regulations, Di- tylenchus destructor Thorne, Globodera pal- lida Stone, G. rostochiensis Wollenweber, Index words: import, nursery plants, quarantine, phytosanitary, dispersal, Meloidogyne, Pratylenchus, Ditylenchus, Tylenchorhynchus, Helicotylenchus, Rolylenchus, Trichodorus 155 JOURNAL OF AGRICULTURAL SCIENCE IN FINLAND https://www.c-info.fi/en/info/?token=-9Dwp2UnN7AqFYMB.fnX71yrpldKaQPdAR1-MxA.aJn3u8HcF21JN7ONObVN4Tj8UAgH68hmNlYM7Hf_cP4Dw0hXuDwDQQRwjb-UicUeT5vmu9bdUGyOG1WIllOeoWzEnoVt-vr87AKeN9dyQad9v_gq1KqqyLL75ye1mhhn8z8DJXqY4g6zlPd140gsc70vf5eRbqDQVgs Radopholus similis (Cobb) Thorne, Xiphine- ma americanum Cobb, D. dipsaci and Meloi- dogyne spp. are included in the A 2 list and Bursaphelenchus xylophilus (Steiner & Buhrer) Nickle together with Nacobbus aberrans (Thorne) Thorne & Allen in the Al list. Im- ported material is supposed to be substantially free from these nematodes. The nematodes of which slight infections are accepted (B list) in- clude Aphelenchoides spp., Pratylenchus con- vallariae Seinhorst, P, penetrans (Cobb) Chitwood & Oteifa and P. vulnus Allen & Jensen. 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 ma- terial 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. Materials and methods Samples Root samples were taken in April 1980 ar- bitrarily 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 trans- ported 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 1970a) for five days to extract the nematodes. The nem- atodes were thereafter fixed in a mixture of formalin, triethanolamineand water (T.A.F.) (Hooper 1970b). The total number of nema- todes and the number of nematodes of the genera Ditylenchus spp., Meloidogyne spp., the spiral nematodes {Helicotylenchus spp., Rotylenchus spp.), Tylenchorhynchus spp., the trichodoridnematodes and the longidorid nematodes were counted. The identifications were done from subsamples mounted in glyc- erol by the Seinhorst slow method (Hooper 1970b). Special attention was paid to species mentioned in the plant quarantine regulations issued in Finland. A sample was defined as in- fected if any of the above nematodes could be detected by either of the two extraction methods. Results Frequency of infections Nematodes belonging to the genera Dity- lenchus, Meloidogyne, Pratylenchus, Helico- tylenchus, Rotylenchus, Tylenchorhynchus and Trichodorus were found in 201 of the 670 investigated root stocks. The number of in- fections specified in the quarantine regulations 156 157 was 115 in 100 stocks. The occurrence of in- fections 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 in- fected 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. Patentilla fruticosa L. Aronia prunifolia Prunus domestica (Marsh.) Rehd. L. Clematis x jack- Prunus padus L. manii T. Moore Rosa L. sp. Picea abies L. Table 1. Occurrence of infections of phytosanitarily important nematodes in the common plant genera imported to Finland in 1980. Plant No Number of stocks infected by st °Jk s D. des. Mel.spp. P. con. P. pen. # Acer L. sp. 20 1 1 Amelanchier Medic, sp. 10 Astible D.Don sp. 12 Herberts L. sp. 18 7 3 Caragana Fabr. sp. 10 Cornus L. sp. 10 1 Hemerocallis L. sp.+ Convallariae L. sp. 10 3 1 Hydrangea L. sp. 11 2 Lonkero L. sp. 10 1 Maius Mill sp. 12 2 Paeonia L. sp. 10 4 1 PhUadelphus L. sp. 10 2 Phlox L. sp. 10 1 Picea A.Dietr. sp. + Pinus L. sp. 13 4 Patentilla L. sp. 14 3 2 Prunus L. sp. 21 1 Rhododendron L. sp. 10 2 Ribes L. +Rubus L. sp. 37 5 2 3 Roso L. sp. 167 1 26 5 5 Salix L. sp. 10 Spiraea L. sp. 15 3 1 Syringa L. sp. 20 4 2 Taxus L. + Thuja L. sp. 10 3 Tiliä L. sp. 12 2 Rosa L. sp. # # 40 4 1 1 Total 512 1 81 10 18 #D. des. = Ditylenchus destructor Mel. spp. = Meloidogyne spp. P. con. = Pralylenchus convallariae P. pen. =P. penetrans # # roses for cut flower production (30) and for house plants (10) Root knot nematodes Meloidogyne infections occurred most fre- quently in the imported plant material (Table 1.). According to the juvenile morphology, the Meloidogyne species included M. arenaria (Neal) Chitwood, M. graminicola Golden & Birchfield, M. hapla Chitwood, M. incognita (Kofold & White) Chitwood, M. javanica (Treub) Chitwood and M. naasi Franklin. The relative frequency within species was not es- timated. Juvenile root knot nematodes were found among the following plants: Acer platanoides L. Aesculus hippo- Pinus cembra L. Populus L. sp. Potentilla fruticosa Rhododendron castanum L. Aronia prunifolia Berberis thunbergii DC. L. sp. Rosa sp. Convallaria majalis L. Cornus alba L. Ribes alpinum L. R. nigrum L. Hemerocallis L. sp. Humulus lupulus L. Hydrangea pani- culata Sieb. Juniperus communis L. Lonicera tatarica L. Lychnis chalcedonica L. Malus baccata (L.) Moench M. x domestica Borkh. Paeonia officinalis L. Parthenocissus guin- guefolia (L.) Planch. Philadelphus coro- narius L. P. x virginalis L. Phlox paniculata L. Physocarpus (Cam- bess.) Maxim, sp. Picea omorica (Panc.) Purk. R. pallidum Otto & A. Dictr. Rubus idaeus L. R. odoratus L. Sorbaria sorbifolia (L.) A.Br. Spiraea L. sp. Syringa L. sp. Symphoricarpos Duham. sp. Taxus cuspidata Sieb. & Zucc. Thuja occidentalis L. Tiliä cordata Mill. Vaccinium corym- bosum L. Viburnum opulus 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 num- ber 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 in- fected. Root lesion nematodes Of the two phytosanitarily important Pra- tylenchus 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. convallariae / groots. No visible symtoms of infections were seen. The other Pratylenchus species, P. crenatus Loof, P. fallax Seinhorst and P. pratensis (de Man) Filipjev were found in 18 plant stocks. The plant species of where Pratylenchus infections were found are as fol- lows: P. penetrans: P. convallariae: Herberts thunbergii Acer ginnala Maxim. Paeonia officinalis Ribes alpinum Potentilla fruticosa Rosa sp. Ribes pallidum Rubus idaeus Rosa sp. Rubus idaeus P. crenatus: Spiraea x cineraria Ajuga reptans Zabel Aesculus hippo- Syringa reflexa castanum L. Schneid. Lonkero tatarica S. vulgaris L. Paeonia L. sp. Viburnum opulus L. Rosa sp. Ribes L. sp. P. fallax: Hydrangea anomala P. pratensis: D. Don Convallaria majalis Thuja occidentalis Rosa sp. About 40 % of the Pratylenchus infections occurred in the roots infected also by Meloi- 158 dogyne spp., but there were no mixed infec- tions between the different Pratylenchus spe- cies. Among roses, infected stocks were found in all types of cultivars: those used for out- door cultivation as well as thosefor cut flower production or for house plants. Ectoparasitic root nematodes Pin nematodes were found in 8 stocks: Paratylenchus bukowinensis Micoletzky in Hydrangea petiolaris and P. projectus Jenkins in Cornus alba. The stylet nematodes Tylen- chorhynchus claytoni Steiner and T. dubius (Butschli) Filipjev were found in 11 stocks, including the following plant species: T. claytoni: T. dubius: Ajuga reptans Astible D. Don sp. Convallaria majaUs ConvaIlaria majat is Cornus L. sp. Rosa sp. Rhododendron sp. Ribes nigrum Rosa sp. Syringa sp. Spiral nematodes were detected in 8 stocks, including several mixed infections of two spe- cies. Helicotylenchus pseudorobustus (Steiner) Golden and H. varicaudatus Yuen occured as follows: H. pseudorobustus: H. varicaudatus: Hydrangea anomala Syringa reflexa Rhododendron sp. The genus Rotylenchus occured as R. fal- lorobustus (Goodey) Sher and R. robustus (de Man) Filipjev: R. fallorobustus: R. robustus: Acer ginnala Astible sp.Astible sp. Aesculus hippo- Rhododendron castanum japonicum Astible sp. Vaccinium corym- Rhododendron japo- bosum nicum (A. Gray) Suring. R. goodeyi: Syringa reflexa Aesculus hippo- castanum The stubby root nematodes Trichodorus spp. were found in four stocks: T. primitivus (de Man) Micotetzky in Patentilla fruticosa and in two stocks of in Rosa rugosa Thumb, and T. viruliferus Hooper in Hydrangea anomala. There were too few nematodes for virus transmission test. Discussion The high frequency of Meloidogyne infec- tions was expected on the basis of the superior international dissemination of these nema- todes (Sasser 1977). Larvae of Meloidogyne spp. where, however, rare in the Danish nur- series and rose fields (Sonderhousen et al. 1968) and equally infrequent further south (Wolny 1980, Kozlowska and Wasilewska 1972). The fairly high frequency of Meloido- gyne 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 coun- tries, or the material was infected during prep- aration 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 Meloi- dogyne infections have not been more fre- quent in local nurseries. In greenhouses, many species of the root knot nematodes can be ex- pected quickly to build up injurious popula- tions. It is thereforeof 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 withM. javanicaby Daulton and Nusbaum (1961) and the abili- ty of Sayre’s M. hapla population to tolerate freezing temperatures (Sayre 1964) are of special concern. 159 The Pratylenchus species described above riods without a host plant (Seinhorst and have, previously, been found in Finland (Sa- rakoski 1978). P. penetrans has caused in- juries 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 nema- todes in the European nurseries (Sonder- housen et al. 1968), might be due to the nematodes’ mobility during harvesting or storage of theplants for import. P. penetrans has shown properties which make it transpor- table (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 po- pulation might become important because of the relatively high infectivity of Pratylenchus species at low temperatures (Ferris 1970, Kimpinski and Willis 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 transpor- tation 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 de- void of any inactive stage can, on the other hand, survive on fungal hyphae. The Para- tylenchus species and T. claytoni are at a cer- tain 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 nemato- des most sensitive to desiccation and to all dis- turbances are the trichodorides (Wyss 1970). T. viruliferus is, however, known to shield it- self 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 po- pulations of the species is unlikely if the in- fections 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 Dar- ling 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). As for the Trichodorus species, the viruses potentially transmitted by them would in- directly make the nematodes economically very important. Neither of the two Tricho- dorus species are known in Finland, but T. primitivus is well distributed in Sweden (Persson 1968). Of the viruses concerned, the existence of tobacco rattle virus (TRY) has been reported in Finnish nurseries (Tapio 1972), but there is no documentation on pea early browning virus (PEBV). 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Nematologische Probleme beim inter- nationalen Handel rail Obstgehölzen. Nachr.bl. Pfl.schutz DDR 32: 230—234. Brzeski, M.W. 1976. Paratylenchus bukowinensis. C.I.H. Descriptions of Plant-parasitic Nematodes. Set 6, No. 79. 2p. Cairns, E.J. 1953. A culture-reared, plant parasitic nematode suitable for teaching and research. Phyto- path. 43: 105. Caveness, F.E. & Jensen, H.J. 1955. Modification ot the centrifugal-flotationtechnique for the isolation and con- centration of nematodes and their eggs from soil and plant tissue. Proc. Helminthological Soc. Wash. 22: 87—89. Gotten, J. & Roberts, H. 1981. Root-lesion nematodes (Pratylenchusspp.) in raspberry-cane beds entered for certification in England. PI. Path. 30: 101—lO4. Daulton, R.A. & Nusbaum, C.J. 1961. The effect of soil temperature on the survival of the root-knot nematodes Metoidogyne javanica and M. hapla. Nematologica 6: 280—294. Esser, R.P. 1978. How nematodes in plant tissue enter and disperse in Florida nurseries, Fla. Dept. Agric. & Consumer Services Div. PI. Ind. Nematology Circ. 43. 2 p. Faulkner, L.R. & Darling, H.M. 1961. Pathological histology, hosts, and culture of the potato rot nema- tode. Phytopath. 51: 778—786. Ferris, J.M. 1970. Soil temperature effects on onion seedling injury by Pratylenchus penetrans. J. Nema- tology 2: 248—251. Hooper, D.J. 1970 a. Extraction of nematodes from plant material. In Southey, J.F. (Ed.) Laboratory methods for work with plant and soil nematodes. Min. Agric. Fish. Food Techn. Bull. 2. p. 34—38. 1970 b. Handling, fixing, staining and mounting nematodes. In Southey, J.F. (Ed.) Laboratory methods for work with plant and soil nematodes. Min. Agric. Fish. Food Techn. Bull. 2. p. 39—54. Johnson, P.W. & Potter, J.W. 1980. Winter survival of root-knot nematodes (Metoidogyne incognita and M. hapla) under selected host crops in southern Ontario. Can. J. PI. Sci, 60: 203—207. Kimpinski, J. & Willis, C.B. 1981. 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SELOSTUS Kasveille haitallisten ankeroisten esiintyminen maahantuodussa taimimateriaalissa vuonna 1980 Sirpa Kurppa Maatalouden tutkimuskeskus, tuhoeläinosasto, 31600 Jokioinen Tutkimuksen tarkoituksena oli selvittää haitallisen an- keroissaastuntojen leviämistä tuotaessa maahamme tai- mituotteita. Kasvieriä tutkittiin kaikkiaan 670 ottamalla jokaisesta yksi näyte. Kasvierät olivat peräisin 42 tuon- tierästä. Haitallisia ankeroislajeja tavattiin 201 kasvi- erässä. Karanteenimääräysten alaisia lajeja löydettiin 100 kasvierästä. Nämä saastunnatkeskittyivät 26 tuontierään, joista 15 erästä löytyi 3 tai useampia saastuneita kasvi- eriä. Juuriäkäraäankeroiset olivat yleisimpiä saastuntojen ai- heuttajia, Niitä löytyi 40 kasvilajista ja 81 kasvierästä, 12 % tutkituista kasvieristä. Saastunnat olivat varsin ylei- siä mm. happomarjapensaissa japioneissa. Eniten saas- tuntoja tuli kuitenkin avomaalle tarkoitetuissa ruusuis- sa, joiden tuontikin oli runsainta. Äkämäankeroissaas- tuntoja tuli myös äitienpäiväruusuissa, mutta leikkoruu- sujen 41 juurierässä löydettiin vain yksi saastunut.Eri äkä- mäankeroislajien esiintymisyleisyyttä ei määritetty. Juurihaava-ankeroista, P. penetrans, tai sen sukulais- lajia P. convallariae löytyi 28 kasvierästä, eli 4 %:sta tut- kituista eristä. Enimmät saastunnat löytyivät ruusuista, vadelmista ja happomarjapensaista. Lahoankeroista, D. destructor, löytyi vain yhdestä ruusuerästä. Juurten pinnalla eläviä, sukuihin Paratylenchus, Ty- lenchorhynchus, Helicotylenchus and Rolylenchus kuu- luvia lajeja löytyi useita, mutta varsinpieniä määriä. Kah- ta virusten levittäjänä tunnettua Trichodorus-suvun la- jia löytyi vain 4 kasvierästä kaikista kuitenkin niin vä- hän, ettei ankeroisten toimintaa virusten siirtäjänä voitu tarkistaa. Wolny, S. 1980. Nicienie, pasozyty roslin w szkolkach zadrzewieniowych. Zesz. Problemowe Postepow Nauk Roln. 232: 121—132. Wyss, U. 1970. Zur Toleranz wandernder Wurzelnema- toden gegenuber zunehmender Austrocknung des Bo- dens und hohen osmotischen Drucken. Nematologica 16; 63—73. Ms received May 9, 1985 Äkämäankeroisten maahankulkeutumisesta aiheutuva riski todettiin uhkaavaksi. Ainakin pohjoisimman lajin, M. hapla, säilyminen talven yli avomaalla on todennä- köistä ja lisääntyminen mahdollista, sillä toukan kehitys vaatii alle puolet siitä lämpötilojen summasta, joka ker- tyy Etelä-Suomessa useimpina vuosina. Saastuntariski pa- henee, jos tuotujen kasvien jatkokasvatustapahtuu kyl- mältä suojattuna.Pahoilta ankeroissaastunnoilta on sääs- tytty kasvihuoneviljelyksillä sen ansiosta, että leikkoruu- sun tuontijuuret ovat olleet tavallista taimitarhamateri- aalia puhtaampia saastunnoista. Viileisiin oloihin sopeu- tuneena juurihaava-ankeroinen saattaa lisääntyä haital- liseksi vähäisistäkin saastuntalähteistä. Se voi tulla mer- kittäväksi myös levittämällä sienitauteja. Juurten pinta- loisina esiintyvien ankeroisten aiheuttamat saastunnat oli- vat niin heikkoja, ettei niillä voida olettaa olevan suurta merkitystä. Acknowledgments I thank Professor Matti Nuorteva in the Department of Agricultural and Forest Zoology, University of Helsinki for facilities and the officers of the Plant Quarantine Office, especially Jukka Lumme, for technical help. Useful comments were provided by Professor Martti Markkula, Doctor Jorma Rautapää, Annikki Lahtinen and Kari Tiilikkala. This study was financially supported by the foundation: August Johannes and Aino Tiuran Maatalouden Tutkimussäätiö. 162