Nematol. medito (1994), 22: 253-263

1 Scottisb Crop Researcb Institute, Invergowrie, Dundee DD25DA, Scotland, United Kingdom2 Pennsylvania State University Fruit Researcb Laboratory, Bigleroille, PA 17307; USA

3 Istituto di Nematologia Agraria, C.N.R. 70126 Bari, Italy

AN APPRAISAL OF SOME ASPECTS OF THE ECOLOGY OF NEMATODE VECTORSOF PlANT VIRUSES

byT. M. HALBRENDT2. A. T. TONESI. C. E. TAYLORI. and F. LAMBERT13D. JT. F. BROW1,

Summary. Eight Longidorus, one paralongidorus and seven Xiphinema species afe natural vectors of nepoviruses and seven Paratrichodo-rus and four Trichodorus species afe vectors of tobraviruses. Nematode transmitted viruses and their vector nematodes afe restricted in theirdistribution to regions with temperate or Mediterranean c!imates with the natural distributions of the viruses reflecting that of their vectors.In Europe the occurrence of a virus and vector frequently afe loca!ised within a relative!y small area whereas in North America the virusesand/or their vectors afe widespread. Specificity of transmission is indicative of a long association between virus and vector which has beendetermined and maintained by the range of factors influencing the complex nematode-virus-plant interactions. The influence of several eco-logica! factors which may affect these interactions and the geographic distributions of the nematode/virus associations afe reviewed and di-scussed.

veloped specific relationships with nematode species thatfunction as their vectors. Because of their limited mobility,nematode populations tend to be localised in discrete ter-ritorial enclaves in which they become specifically asso-ciated with viruses through interdependent ecological fa-cotrs. Wider distribution occurs when viruses and vectorsbecome associated with cultivated plants, which providethe means far their long distance dissemination in plantmaterial and soil through man's activities. In most situa-tions nepo- and tobra-virus infections in the field afe ap-parent only in crop plants in which symptoms afe relative-ly severe and, in some instances, plant death may occur.By contrast, infection of wild plants is usually symptom-less, indicating an ecologically balanced association. Like-wise, many longidorid and trichodorid vector species bavea wide host range among wild plants but apparently theirfeeding causes little appreciable damage whereas thegrowth of crop plants is often impaired by nematode feed-ing.

Whilst agricultural activities have resulted in the wide-spread dissemination of several vector species, the geo-graphical distributions of most longidorid and trichodoridnematodes afe nevertheless established relative to ecologi-cal facotrs, on a geological timescale. Concurrently, specif-ic associations became established between some of thespecies and their respective nepo-and tobra-viruses. Someof the ecological factors pertaining to the establishment ofvirus and vector associations afe discussed here.

Among the many groups of nematodes that afe par-asites of plants, only a relatively few species of Dorylaimi-da and Triplonchida afe vectors of plant viruses (Jairajpuriand Ahmad, 1992; Hunt, 1993). Currentiy seven Xiphine-ma, eight Longidorus and one Paralongidorus species afenatural vectors of nepoviruses and four Trichodorus andseven paratrichodorus of tobraviruses (Table I). Most vec-tor species afe indigenous to Europe and North America,an exception being L. martini which is associated withmulberry ringspot virus in ]apan. Several Longidorus andXiphinema species, and their associated viruses, bave in-advertentiy been transported by man's activities from theirareas of origin to other regions such as Australasia andNorth America, e.g. X. diversicaudatum with arabis mosaicvirus (AMV) and X. index with grapevine fanleaf virus(GFLV). Trichodorid nematodes afe also widely distributedin ~urope and North America with several species asso-ciated naturally with tabacco rattle virus (TRV), the mostwidespread of the tobraviruses. Again, these viruses andvectors bave been dispersed by man to other countriessuch as ]apan, New Zealand and Brazil. However, pepperringspot virus (PRV) appears to be unique to Brazil, whereit is vectored by P. minor, and the remaining tobravirus,pea early-browning (PEBV), occurs only in localised areasin northern Europe and North Africa (Taylor and Brown,1981; Brown, 1989).

It is now general1y accepted that nepo- and tobravirus-es afe natural1y associated with wild plants and bave de-

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Geographical distribution

Nematode taxa which afe recognized today afe consid-ered to bave been derived from a widespread taxon whichsplit as the continents separated to their present geograph-ical position (Ferris, 1983). From a comparison of taxo-nomic characteristics of longidorid genera, Coomans(1954) concluded that Xipbinema originated in Gondwanaand before the breakup of Pangaea had spread to Laura-sia. Longidorus and paralongidorus afe considered to baveoriginated in Southeast Africa and India, when these twoareas were stili united, and a later spread to Laurasia wasfollowed by a main speciation of Longidorus in the holarc-tic region, especially Europe. Although taxonomic charac-teristics bave been used to identify distinct groupings oftrichodorid species (Loof, 1975; De Waele et al., 1982)these do not indicate evolutionary directions or centres oforigino However, the present distribution of trichodorids isbroadly the culmination of the influence of changing geo-logical events. Man's influence on the geographical distri-bution of species is relatively srnall, probably being rnainlymanifest in outlier populations, and the dispersal of a spe-cies aver large distances, such as world wide dissemina-tion of X. index with grapevine from its presumed centreof origin in Iran (Persia).

The most recent major geological event that has influ-enced nematode distribution is the quatemary glaciationwhich occurred C. 40,000 years ago. In Europe there is amarked decrease, south to north, in species richness (Top-ham and Alphey, 1985) and the present northem limit ofseveral species is clearly demarcated. For example L. mac-rosoma is uniformly distributed throughout France and thelow countries but does not extend northwards beyondsouthem England. This northem boundary has been corre-lated with the mean July 15° isotherm, implying that thespecies has certain ecological temperature requirements(Boag et al., 1991). Also, it has been suggested(Dalmasso,1970; McNamara and Flegg, 1981) that L. macrosoma pop-ulations which survived the period of glaciation were un-able to spread northwards because of the destruction ofthe deciduous forests, which provided hosts far the spe-cies, during the bronze and iron ages. Xipbinema diversi-caudatum is another example of a longidorid specieswhich is widely distributed in Europe but with a clearlydemarcated northem boundary in Scotland far which thereafe no obvious climatic or edaphic reasons (Topham andAlphey, 1985); the frequency of occurrence of the speciessuggests that its slow northerly diffusion has not yet beencompleted. Although these interpretations of geographicaldistribution afe highly conjectural they nevertheless indi-cate some of the ecological parameters that influence spe-ciation within the broad ranges of ancestral species. Unfor-tunately, little is known about the ecological requirementsof the majority of longidorid and trichodorid nematodes

and elucidation of speciation and species diversity has cur-rently to be approached on the groupings of morphomet-ric characters.

Western Europe appears to be a region of well estab-lished nematode species and with relatively graduaichange in distribution and speciation. However, the east-ero Mediterranean countries present a complexity of longi-dorid and trichodorid species that possibly reflects thegeological history of the region, with the formation, duringthe Miocene, of microcontinents movement between themajor plates of Africa and Eurasia (McKenzie, 1970 in Top-ham and Alphey, 1985).

The present geographical distribution of Xipbinemaand Longidorus species in Europe and the Mediterraneanregion (Alphey and Taylor, 1986; Brown and Taylor, 1987)has been quantitatively analyzed by Navas et al., (1990).They recognized two main groups of species, the Europe-an-Atlantic and the Mediterranean. Furthermore, they con-sidered the distribution of Xipbinema species to be a rela-tively recent dispersion process, with the pleisochoric lim-its of the genus in the southern Mediterranean region andthat of Longidorus, with a relatively early dispersal, in thenorthern Mediterranean and southern European countries.In a more detailed appraisal of the distribution of Longid-orus species in Euromediterranea, Navas et al. (1993) iden-tified the centres of distribution of 32 species within dis-tinctive geographical regions (chorological units). They hy-pothesized, inter alia, that after glaciation the founder spe-cies L. intermedius, L. africanus and L. congoensis werethe origin of dispersive speciation throughout much of Eu-romediterranea.

Longidorids and trichodorids present in North Americaafe largely distinct from those species present in Europeand other continents. Also, there is an apparent paucity ofLongidorus species in North America; of the ten species re-ported only seven afe probably indigenous, the three oth-ers having been introduced with planting material. Thiscompares with more than 50 species reported from Europe.In contrast, 38 species of Xipbinema have been identifiedin North America of which more than half have probablybeen introduced compared with at least 60 species in Eu-rape (Robbins and Brown, 1991; Robbins, 1993). Howev-er, the apparent paucity in North America of the large Xi-pbinema and Longidorus,species has been partly attribut-ed to inappropriate nematode extraction procedures beingemployed there and it seems probable that many new spe-cies will be discovered in the future (Robbins and Brown1991; Robbins, 1993).' For example, far 60 years the mostwidespread longidorid occurring in North America wasidentified as Xipbinema americanum. However, a taxo-nomic reappraisal of populations previously identified asX. americanum resulted in f1fteen new species being de-scribed to give a complex of 25 morphologically similar,parthenogenetic species (Lamberti and Bleve-Zacheo,

254

19911960

X. diversicaudatum I 200g

_>50

~>25

~>12

~>6

[28>2

(=:]<1

[))I:;J

al)

~

30

(/)-oL-Cù

>-

- ., '"

20

: :-:-~:: .

10:-~~-~-~I

oHedgeHedge

Fig. 1 - l11e distribution of Xipbinema diversicaudatum in a mixed woodland at Geesecroft, southern England. A, in 1960 (data from Harri-

san and Winslow, 1961); B, in 1991 (after Taylor et al., 1994).

the populations into rive subgroups. Their X. americanumsubgroup consisted primarily of North American species;X. pachtaicum subgroup mainly of European species; X.lambertii subgroup mainly of Asian species; X. brevicollesubgroup, comprising seven species has a cosmopolitandistribution and the X. taylori subgroup containing onlytwo species, one each from Europe and North America.

The species of Xiphinema and Longidorus indigenousto Africa, Europe and North America form distinct conti-nental groups. This also applies to the nematode transmit-ted nepoviruses indigenous to Europe and North America.Indigenous species of Trichodorus and Paratrichodorusdiffer between North America and Europe, and althoughtabacco rattle virus occurs in both continents and is trans-mitted by some of the species, the North America strainsof the virus afe serologically distinct from those in Europe(Oswald and Bowman, 1958; Cadman, 1963).

1979). Currently 20 of the 39 X. americanum-group spe-cies bave been described from specimens originating fromNorth America (Robbins and Brown, 1991; Robbins, 1993).

Halbrendt and Brown (1992, 1993) recently reportedthat several Xipbinema americanum-group species fromEurope bave four juvenile stages, which is considered nor-mal far Nematoda, but that populations from North Ameri-ca bave only three such stages. These North Americanpopulations afe vectors of three North American nepovi-ruses (Brown et al., 1993, 1994b). Using Restriction Frag-ment Length Polymorphism with 16 populations of X.americanum-group nematodes Vrain (1993) distinguishedfour groups of populations representing X. americanum,X. rivesi, X. pacificuml X. californicum and X. bricolense.Lamberti and Ciancia (1993) studied the morphometrics of49 populations of 39 species attributed to the X. ameri-canum-group and by hierarchical cluster analysis placed

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-."-r-;:!".\J'. - '.-

The apparent effectiveness with which some specieshave been widely dispersed by man or by natural meansindicates that they have genetic and ecological flexibilitye.g. wide host range, adaptability to a range of soil types,and reproduction sustained aver a broad temperaturerange. It may be expected that isolation of populations indiverse biotopes would result in reproductive isolation andhence the establishment of new species. When Brown andTopham (1985) examined X. diversicaudatum specimensthat were obtained from populations widely distributedthroughout the world they found morphological and mor-phometric differences between populations, but they didnot regard these differences as sufficient to distinguishpopulations as separate species. Subsequently, this conclu-sion was validated when it was demonstrated that many ofthese populations could interbreed successfully with apopulation from Scotland (Brown, 1986a).

Dalmasso and Berge (1983) presented a hypotheticalmodel to explain evolution in the Longidoridae in whichpopulations of ancestral amphimictic forms (species) couldbe affected by inbreeding resulting in complete homozy-gosity, subsequent facultative meiotic parthenogensis witha resulting loss of males, and finally mutations giving riseto "clona!" species. These "clona!" species would be mor-phologically similar within species complexes. Severalsuch groups afe evident rodar, far example, populationsof X. coxi from Florida, USA, were recognized as distinctfrom those in Europe (Dalmasso, 1970; Taylor and Brown,1976) to the extent that Sturhan (1984) recognized twospecies, X. pseudocoxi and X. coxi, with the latter dividedinto two sub-species (Brown and Taylor, 1987). Morpho-metric differences between dispersed populations have al-so been noted in L. elongatus, L. profundorum and L. vi-neacola. Such differences should also be considered in re-lation to their effect on the efficiency of virus transmission,as it has been demonstrated with populations of X. diversi-caudatum (Brown and Taylor, 1981; Brown and Trudgill,1983; Brown, 1985, 1986b) and in populations of X. ameri-canum sensu lato (Griesbach and Maggenti, 1989). How-ever, there is no evidence that differences in the ability totransmit viruses provide a basis far distinguishing speciesor populations of a vector.

Persistence of Nematode Populations and Viruses

A characteristic of nematode transrnitted viruses is theirpersistence at sites far long periods, even in the absenceof virus infectible crop hosts. This is dependant bolli onthe survival of the vector population, particularly in situa-tions where the soi! is cultivated and where crops afe ro-tated, and on the presence of virus-infected weed seedsand/or perennial plants. A study of two populations of X.diversicaudatum spanning 30 years provided data onsome of the ecological factors involved.

In 1961 the distribution of a population of X. diversi-caudatum was rnapped in an undisturbed, mixed wood-lanci at Geesecroft, southern England (Harrison and Win-slow, 1961) and in 1966 and 1967 that of another popula-tion. in an arable field at Gilliesfaulds, eastern Scotland(Taylor and Thornas, 1968). Resampling at Geesecroft in1991 revealed the horizontal distribution of the nernatodepopulation to bave remained virtually unchanged in theintervening years (Fig. 1; Taylor et al., 1994). A reductionin the numbers of nematodes, by two thirds from levelsdetected in 1961, was believed to bave resulted from a se-rious rainfall deficit in preceding years and the increaseddensity of the woodland canopy which had reduced theweed flora and hence the hosts far nematodes in theupper soillayers which were sampled. At Gilliesfaulds, thenernatode infestation was presumed to bave originated ina hedge bordering the eastern perimeter of the field andwhen sampled in 1966, and again in 1967, had spreadabout 35 metres into a raspberry crop cv. Malling Jewel(Fig. ZA). By 1991, the pattern of infestation could stilI berelated to that evident in 1967 but had become scatteredinto sub-populations with some spread westwards into theremainder of the cultivated area (Fig. 2B). Continuous cul-tivation and change in crops during the intervening yearswould be expected to bave some adverse effect on thenematodes as well as affecting their horizontal distribution.The largest sub-population recorded in 1991 was in a grassstrip at the northern part of the field which, since 1986,had provided a good host far the nernatode and an undis-turbed habitat.

In 1966 the raspberry crop at Gilliesfaulds was infectedwith SLRV but not AMV, to which it is immune, althoughthe latter virus was detected in several weed species. In1991, after several crop rotations including the planting ofSLRV-immune raspberry cv. Glen Moy, in 1987, only AMVwas detected in soil samples and in some weed species(Taylor et al., 1994). The virus was present as two strains,differing in the severity of symptorns induced in herba-ceous plants, indicating that the natural weed bank is anefficient reservoir far preserving nepoviruses and their var-iants that occur naturally. Weed seed transmission of ne-po- and tobra-viruses has been well documented as pro-viding an alternative strategy far virus persistence in na-ture with up to 100% of seed from an infected motherplant being infected and capable of survival in soil farrnany years (Murant, 1983).

The existence of two variants of AMV with a popula-tion of X. diversicaudatum is an example of a strategy farthe survival of nematode transmitted viruses in nature.Other examples of several variants of a virus occurringnaturally together with a vector population bave been re-ported far AMV and X. diversicaudatum from strawberryin Norway; RRV and L. elongatU$ from raspberry in easternScotland Qones et al., 1989) and TRV with T cylindricU$

2'iC1 -

T ABLE I - Specific associations between Longidorus, Paralongidorus, Paratrichodorus, Trichodorus and Xiphinema virns-vectornematode species and nepo- and tobra-virnses.

Vector species Viruses Acronym Reference

L. apulus AILV Rana and Roca, 1973

CRDVTBRV

Brown et al., 1994a

Harrison, 1964

L. anhensisL. attenuatus

L. diadecturusL. elongatus

PRMVRRV

Eveleigh and Allen, 1982

Taylor, 1962

TBRV Harrison et al.. 1961

Roca et al.. 1982L. fasciatus AILV

Harrison, 1964L. macrosoma RRV

MRV

RRV

L. mal1iniP. maximus

Yagita and Komuro, 1972Jones et al., 1994

CRLVPRMVTobRSVTornRSVCRLVTobRSVTornRSVTornRSVCRLVTobRSVTornRSVAMVSLRVGFLVGFLVCRLVTobRSVTornRSV

X. americanum(sensu lato ~

X. americanum(sensu stricto.->

X. brlcolenseX californicum

X. diversicaudatum

NEPOVIRUSES

artichoke ltalian latent(Italian strain)cherry rosette diseasetornato black ring(German/English strain)peach rosette rnosaic

raspberry ringspot(Scottish strain)tornato black ring(Scottish strain)artichoke ltalian latent(Greek strain)

raspberry ringspot(English strain)

rnulberry ringspotraspberry ringspot(German grapevine strain)cherry rasp leafpeach rosette rnosaictabacco ringspottornato ringspotcherry rasp leaftabacco ringspottornato ringspottornato ringspotcherry rasp leaftabacco ringspottornato ringspotarabis rnosaicstrawberry latent ringspotgrapevine fanleafgrapevine fanleafcherry rasp leaftabacco ringspottornato ringspot

X. indexX. italiaeX. rivesi

Nyland et al., 1969Klos et al., 1967Fulton, 1962Breece and Hart, 1959Brown and Halbrendt, 1992Brown and Halbrendt, 1992Brown and Halbrendt, 1992Brown and Halbrendt, 1992Brown and Halbrendt, 1992Brown and Halbrendt, 1992Hoy et al., 1984Jha and Posnette, 1959Lister, 1964Hewitt et al., 1958Cohn et al., 1970Brown and Halbrendt, 1992Brown and Halbrendt, 1992Forer et al., 1981

TOBRAVIRUSES

P. anemones rea early-browningtabacco rattle

pepper ringspottabacco rattletabacco rattle

rea early-browningtabacco rattle

PEBVTRVPRVTRVTRVPEBVTRV

P. minor(syn. cbristiet)P. nanusP. pacbydermus

Harrison, 1967Hoof, 1968Salomao, 1973Walkinshaw et al., 1961Cooper and Thornas, 1970

Hoof, 1962Gibbs and Harrison, 1964b

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Viruses Acronvm ReferenceVector species

tabacco rattle Ayala and Allen, 1968P. tansaniensis(syn. allius)P. teres

TRV

rea early-browningtabacco rattletabacco rattletabacco rattle

rea early-browningtabacco rattletabacco rattle

rea early-browningtabacco ratde

PEBVTRVTRVTRVPEBVTRVTRVPEBVTRV

P. tunisiensisT cylindricusT. primitivus

Hoof, 1962Hoof, 1964Roca and Rana, 1981

Hoof, 1968Gibbs and Harrison, 1964aSanger, 1961Cremer and Schenk, 1967Gibbs and Harrison, 1964aHoof et al., 1966

T. similisT. viruliferous

. Unequivocal identification of species not av~ilable or prior to the review of the X. americanum-group (Lamberti and Bleve-Zacheo, 1979).

.. Species identification determined by using individuai nematodes in virus transmission studies (Brown and Halbrendt, 1992; Brown et al.,

1994h)

highly specific associations with their vectors. Specificity oftransmission is most evident in the European context,where a particular virus, or a serologically distinct strain,can be transmitted by one species but not by another. Forexample, AMV is transmitted by X. diversicaudatum butnot by any other species tested, Scottish strains of RRV andTBRV afe transmitted by L. elongatus but English strains ofthese viruses by L. macrosoma and L. attenuatus, respec-tively, and a strain from grapevine in Germany Qones etal., 1994) by P. maximus but not by L. macrosoma. Speci-ficity of transmission is also evident with TRV with manyof the strains associated with different vector species(Ploeg et al., 1992).

In North America, X. amerlcanum has been implicatedas a natural vector of CRLV, PRMV, TobRSV and TomRSV(Breece and Hart, 1959; Fulton, 1962; Klos, et al., 1967;Nyland et al., 1969) and X rlvesi and X. californicum asvectors of TomRSV (Forer et al., 1981; Hoy, et al., 1984;Table I). This indicates little specific transmission ofTomRSV by several members of the X. americanum-groupand that X. americanum is unusual in being a vector ofeach of the four indigenous North American nematodetransmitted nepoviruses. Some of this apparent lack ofspecificity may be a result of uncertainty in species iden-tification prior to a reappraisal of the taxonomy of the X.amerlcanum-group (Lamberti and Bleve-Zacheo, 1979)and of the characterisation of the specific virus strainstransmitted. However, Brown and Halbrendt (1992) andBrown et al. (1993, 1994b) using individuaI nematodesfrom three populations of X. americanum sensu strlcto, X.brlcolense, X. californicum and X. rlvesi showed that X.amerlcanum, X.. californicum and X. rlvesi transmittedCRLV, TobRSV and two strains of TornRSV but that X. rlve-si transmitted the viruses more frequently. Xiphinema brlc-

olensis transmitted only TomRSV. These data confinn a rel-ative lack of specificity between North American nematodetransmitted nepoviruses and some of their vectors.

Martelli and Taylor (1989) speculated that vector popu-lations widely separated geographically might be expectedto differ in their ability and efficiency to transmit viruses.This could result from ecological pressure on the virus toadapt to its plant host, whereby if the dominant host werean annual, or short tenn perennial, selection pressure farfrequent (= efficient) transmission would be selected toensure survival of the virus; whereas with long tenn per-ennials, such as fruit trees, such pressure would be muchless and relatively infrequent (= inefficient) transmissionby vectors might result. Ecologically driven selection pres-sure can be presumed to be more likely in disturbed (cul-tivated) than in undisturbed habitats. Viruses afe also sub-ject to selection pressure because of the changing flora, aswell as biological modifications in the nematodes, and evi-dence far this may be assumed from the range of virusstrains which occur. Thus, the type British strain of SLRV isefficiently transmitted by several geographically disparatepopulations of X. diversicaudatum but only infrequentlyby populatioI1s from France, ltaly and Spain, whereas ser-ologically distinguishable strains of SLRV from Italy weretransmitted consistently only by a population of the vectorfrom Italy, and then only infrequently (Brown and Taylor,1981; Brown and Trudgill, 1983; Brown, 1985, 1986b).

Recently, specificity of transmission of serologicallydistinguishable strains of tobraviruses with trichodoridnematodes has been demonstrated (Ploeg et al., 1992).Tobraviruses occur naturally as a range ofserotypes whichin Europe have been shown to be transmitted each by adifferent nematode species e.g. isolates of the PRN sero-type of TRV from Britain, Sweden and the Netherlands afe

- 259 -

transmitted. only by P. pacbydermus. In North America,where only Paratricbodorus species bave been reportedas vectors of TRV, it is uncertain if specificity of transmis-sion occurs with TRV isolates and populations/species of(oara )trichodorid nematodes.

Mechanisms lnvolved in Virus and Vector Associations

rus particles is believed to involve the interaction of com-plementary molecules at their point of contact, such as oc-curs in many host-pathogen systerns and in other biologi-cal situations where "self' and "non-self' bave to be recog-nized.

There is some evidence of "finger-like" structures atthe end of TRVparticles that may be involved in the specif-ic association with the vector (Legorboru, 1993). Biochemi-cal evidence from nepoviruses indicates differences inpolypeptide sequences adjacent to the N-terminai side ofthe coat proteins which could account far some aspects ofspecific association between 'virus and vector species(Block et al., 1992).

Specificity of the virus/vector association, which prob-ably developed during a long association of the vectorswith their associated viruses, implies at its siniplest a "genefar gene" type of recognition processo Although in manyinstances the same part of the coat protein appears to becrucial far both specificity of retention and antibody recog-nition, this is not so far ali nematode and virus associa-tions. For example, a population of L. attenuatus fromBritain transmitted two serologically distinguishable Britishisolates of TBRV much more efficiendy than two isolatesfrom Germany (Brown et al., 1989), implying that efficien-ciy of transmission is correlated more strongly with geo-graphic origin than antigenic relatedness. Nevertheless,more substantive serological differences afe usually asso-ciated with differences in the vector species. Thus two ser-ological1y distinct strains of artichoke Italian latent nepovi-rus from Italy and Greece afe transmitted by L. apulus andL. fasciatus, respectively (Table I). Siniilarly, the Germanand Scottish serotypes of TBRV afe transmitted specifical1yby L. attenuatus and L. elongatus, respectively. The Scot-tish and English serotypes of RRV afe transmitted most ef-ficiendy by L. elongatus and L. macrosoma, respectively,but each species can transmit the other virus, albeit le~sef-ficiendv.

Electron microscopy has provided evidence far thesites of virus retention in nematode vectors. In Longidornsspecies the virus particles afe apparently adsorbed in asingle layer to the inner surface of the odontostyle, and inL. elongatus particles of RRV or TBRV may also be locatedbetween the odontostyle and the guiding sheath (Taylorand Robertson, 1969). In contrast Xipbinema vectors havenepovirus particles specifically associated with the cuticu-lar lining of the odontophore and the oesophagus (Taylorand Robertson, 1970a). In trichodorid vectors TRV particlesafe retained in association with the lining of the food ca-nal from the anterior region of the oesophostome to theoesophago-intestinal valve, but afe not attached to the on-chiostyle (Taylor and Robertson, 1970b).

Experiments with pseudo-recombinant isolates of somenepo- and tobraviruses have demonstrated that the associ-ation between vector and virus is determined by the RNA-2 of the bipartite virus genome (Harrison et al., 1974; Har-rison and Murant, 1977; Ploeg et al., 1993). As RNA-2 alsodetermines the production of the virus protein coat, itseems reasonable to assume that the specific associationbetween virus and vector involves some properties of theprotein coat and the cuticular surfaces at the sites of reten-tion within the nematode vector. However, the precise na-ture of this association has stilI to be determined and thereis some circumstantial evidence that this may not be thesame far virus/vector associations.

In Longidorus vectors a strong negative charge ispresent on the exterior surface of the odontostyle and it isspeculated that positively charged virus particles ingestedby the nematode with plant sap afe attracted to the nega-tively charged surface of the odontostyle. It is further spec-ulated that different strains of the same virus would havedifferent surface charge densities, thus requiring differentvector species, but that two different viruses transmitted bythe saITl,e vecotr species, e. g. RRV and TBRV by L. elonga-tus, would have similar charge densities (Taylor andBrown, 1981). In Xipbinema it has been shown that a dis-continuous layer of carbohydrate lines the odontophoreand oesophagus and virus particles attach only in thesezones (Robertson and Henry, 1986). Similarly, in P. pacby-dermus and presumably in other trichodorid vectors, therotai wall of the food canal stains far carbohydrates andthe meehanism of virus retention is similar to that far Xi-pbinema species. The nature of the attachment of the vi-

Conclusion

In Europe, vector species and their associated virusesafe considered to bave developed a high degree of speci-ficity of virus transmission. In North America fiere is evi-dence of much less specificity of transmission at the spe-cies level, but differences bave been recorded betweenpopulations. Thorough taxonomic reappraisal of the groupand further precise transmission experiments will help toelucidate the nature of the associations between NorthAmerican nepo- and tobra-viruses and their associatedvectors.

It may be concluded that a close association has devel-oped between virus and vector that is nevertheless ca-pable of adjustment to the changing ecological selection

7hO -

pressures that influence the different components of thenematode-virus-plant interaction. Although generalisationsmay be made about nematode transrnission of plant virus-es each virus and vector association has elements ofuniqueness that afe a constant reminder of the gaps in ourknowledge and the inevitability of change in biological sit-uations. due to nature itself or to rnan's activities.

This is an extended version of an invited paper deliv-ered at the Intemational Society of Plant pathologists, PlantVirus Epidemiology Intemational Symposium - Virnsesand tbe Environment, 27 - 30th July, 1992, Valenzano, Ba-ri, Italy. Research at the Scottish Crop Research Institute isgrant-aided by the Scottish Office Agriculture and FisheriesDepartment (SOAFD). Non-indigenous populations ofnematodes and virus isolates were held under licence fromSOAFD. This study was completed with financial assis-tance received by two of us (DJFB and FL) from the Consi-glio Nazionale delle Richerche, Italy and the British Coun-ci!, Great Britain, as part of a Bi!tateral Agreement.

Literature cited

ALPHEY T. J. W. and TAYLOR C. E., 1986. European Atlas ofthe Lon-gidorldae and Trlchodorldae. Scotto Crop Res. Inst., Dundee,

&otland, pp. 123.AYALA A. and ALLEN M. W., 1968. Transmission of the Califomian

tabacco rattle virus by three species of the nernatode genusTrlchodorus. J. Agrlc. Univo Puerto Rico, 52: 101-125.

BWCK V. C., WARDE~J., Jo~Y C. A., MANoUKIAN A., ROBINSON D. J.,EDWARDS M. L. and MAYO M. A., 1992. The nucleotide se-quence of RNA-2 of raspberry ringspot nepovirus. J. Cen. Vir-

01., 73: 2189-2194.BOAG B., CRAWFORD J. W. and NEIlSON R., 1991. The effect of glo-

bal wanning on the geographical distribution of plant parasit-ic nernatodes. Nematologica, 36: 312-323.

BREECE J. R. and HART W. H., 1959. A possible association of nem-atodes with the spread of peach yellow bud mosaic virus. Pl.

Vis. Reptr., 43: 989-990.BROWN D. J. F., 1985. The transrnission of two strains of strawber-

ry latent ringspot virus by populations of Xiphinema diversi-caudatum (Nematoda: Dorylaimida). Nematol. medit., 13:

217-223.BROWN D. J. F., 1986a. Reproduction and interbreeding within and

between populations of Xiphinema diversicaudatum (Nerna-toda: Dorylaimoidea). Nematol. medit., 14: 73-83.

BROWN D. J. F., 1986b. The transrnission of two strains of arabismosaic virus tram Engiand by populations of Xiphinema di-versicaudatum (Nernatoda: Dorylairnida) tram ten countries.

Rev. Nematol., 9: 83-87.BROWN D. J. F., 1989. Viruses transrnitted by nernatodes - EPPO!

OEPP Bull., 19: 453-461.BROWN D. J. F., GRUNDERJ., HOOPER D. J., KLiNGLERJ. and KUNZ P.,

1994a. Longidorus arthensis sp. n. (Nematoda: Longidoridae)a vector of cherry rosette disease caused by a new nepovirusin cherry trees in Switzerland. Nematologica, 40; 133-149.

BROWN D. J. F. and HALBRENDT J. M., 1992. The virus vector poten-tial of Xiphinema amerlcanum and related species. J. Nema-fol.. 24: 584.

BROWN D. J. F., HALBRENDT J. M., JONES A. T., VRAIN T. C. and ROB-BINS R. T., 1994b. Transmission of three North Arnerican nepo-viruses by populations of four distinct Xipbinema american-um-group species (Nernatoda: Dorylaimida). Pbytopatbology84: 646-649.

BROWN.D. J. F., HALBRENDT J. M., ROBBINS R. T. and VRAIN T. C.,

1993. Transmission of nepoviruses by Xipbinema american-um-group nematodes. f. Nematol., 25: 349-354.

BROWN D. J. F., MURANT A. F. and TRUDGILL D. L., 1989. Differencesbetween isolates of the English serotype of tornato black ringvirus in their transmissibility by an English population of Lon-gidorus attenuatus (Nernatoda: Dorylaimoidea). Rev. Nema-tol., 12: 51-56.

BROWN D. J. F. and TAYLOR C. E., 1981. Variazioni nella trasmis-sione di virus tra popolazioni di'nematodi vettori Longidori-dae. Atti. Soc. ltal. Nematol., Giornate Nematol., Firenze 28-29novembre, 1979, pp. 191-204.

BROWN D. J. F. and TAYLOR C. E., 1987. Comments on the occur-rence and geographical distribution of longidorid nernatodesin Europe and the Mediterranean region. Nematol. medit., 15:333-373.

BROWN D. J. F. and TOPHAM P. B., 1985. Morphometric variabilitybetween populations of Xipbinema dive~icaudatum (Nerna-toda: Dorylairnoidea). Rev. Nematol., 8: 15-26.

BROWN D. J. F. and TRUDGILL D. L., 1983. Differential transmissibil-ity of arabis mosaic and strawberry latent ringspot viruses bythree poplations of Xipbinema dive~icaudatum from Scot-lanci, ltaly and France. Rev. Nematol., 6: 229-238.

CADMAN C. H., 1963. Biology of soil-borne viruses. Ann. Rev. Pby-topatb., 1: 143-172.

COHN E., TANNE E. and N1TZANY F. E., 1970. Xipbinema italiae, anew vector of grapevine fanleaf virus. Pbytopatbology, 60:181-182.

CooMANS A. V., 1985. A phylogenetic approach to the classitìca-tion of the Longidoridae (Nernatoda: Dorylaimida). Agric. Eco-syst. Environ., 12: 335-354.

COOPER J. I. and THOMAS P. R., 1970. Tricbodorus nanus, a vectorof tabacco rattle virus in Scotland. Pl. Patb., 19 197.

CREMER M. G. and SCHENK P. K., 1967. Notched leaf in Gladiolusspp., caused by viruses of the tabacco rattle virus group.Netb.f. Pl. Patb., 73: 33-48.

DALMASSO A., 1970. Influence directe de quelques facteurs ecolo-giques sur l'activité biologique et la distribution des especesFrancaises de la famille des Longidoridae (Nernatoda: Dorylai-mida). Ann. Zool. Ecol. Anim., 2: 163-200.

DALMASSO A. and BERGE J. B., 1983. Enzyme polymorphism and theconcept of parthenogentic species, exemplified by Meloidogyne,pp. 187-196. In: A. R. Stalle, H. M. Platt and L. F. Khalil (Eds).Concepts in nernatode systernatics, London: Academic Presso

DE WAELE D., MANoNi G., ROCA F. and LAMBER11 F., 1982. Tricbod-orus taylori sp.n. (Nernatoda: Dorylairnida) from ltaly. Nema-tal. medit., 10: 27-37.

EVELEIGH E. S. and ALLEN W. R., 1982. Description of Longidorusdiadecturus n. sp. (Nernatoda: Longidoridae), a vector of thepeach rosette mosaic virus in peach orchards in southwesternOntario, Canada. CanI. Zool., 60: 112-115.

FERRIS V. R., 1983. Phylogeny, historical biogeography and thespecies concept in soil nematodes, pp. 143-161. In: A. R.Stalle, H. M. Platt and L. F. Khalil (Eds). Concepts in nerna-tode systernatics. London: Academic Presso

FORER L. B., WILL N. and POWELL C. A., 1981. Xipbinema rivesi, anew tornato ringspot virus vector. Pbytopatbology, 71: 874.

FULTON J. P., 1962. Transmission of tabacco ringspot virus by Xi-pbinema americanum. Pbytopatbology, 52: 375.

GIBBS A. J. and HARRISON B. D., 1964a. A formar rea early-brown-ing virus found in Great Britain. Ann. appl. Biol., 54: 1-11.

2(:)1

GIBBS A. J. and HARRISON B. D., 1964b. Nernatode-transmitted vi-ruses in sugar beet in East Anglia. Pl. path., 13: 114-150.

GRIESBACH J. A. and MAGGEN"n A. R., 1989. Vector capability of Xi-phinema americanum sensu lato in Califomia. f. Nematol.,21: 517-523.

HALBRENDT J. M. and BROWN D. J. F., 1992. Morphometric evidencefar three juvenile stages in some species of Xiphinema ameri-canum sensu lato. f. Nematol., 24: 305-309.

HALBRENDT J. M. and BROWN D. J. F., 1993. Aspects of biology anddevelopment of Xphinema americanum and related species.f. Nematol., 25: 355-360.

HARRISON B. D., 1964. Specific nematode vectors far serologicallydistinctive forms of raspberry ringspot and tornato black ringviruses. Virology, 22: 544-550.

HARRISON B. D., 1967. Pea early-browning virus (PEBV). Ann Rep.far 1966. Rothamsted Exp. SIn. England., p. 115.

HARRISON B. D., MOWAT W. P. and TAYLOR C. E., 1961. Transmis-sion of a strain of tornato black ring virus by Longidorns elon-gatus(Nernatoda). Virology, 14: 480-485.

HARRISON B. D. and MURANT A. F., 1977. Nernatode transmissibilityof pseudorecombinant isolates of tornato black ring virus.Ann. appl. Biol., 86: 209-212.

HARRISON B. D., MURANT A. F., MAyo M. A. and ROBERTS I. M.,1974.. Distribution of determinants far symptom production,host range and nematode transmissibility between the twoRNA components of raspberry ringspot virus. f. Cen. Virol.,22: 233-247.

HARRISON B. D. and WINSLOW R. D., 1961. Laboratory and fieldstudies on the relation of arabis mosaic virus to its nematodevector Xphinema dive~icaudatum (Micoletzky). Ann. appl.Biol., 115: 57-69.

HEWI1T W. B., RAsKI D. J. and GOHEEN A. C., 1958. Nernatode vectorof soil-home virus of grapevines. Phytopathology. 48: 586-595.

HOOF H. A. van., 1962. Trichodorns pachydermus and T. teres,vectors of the early-browning virus of peas. Tijdschr. Plziek-ten, 68: 391-396.

HOOF H. A. van., 1964. Trichodorns teres a vector of rattle virus.Neth.f. P/. path., 70; 187.

HOOF H. A. van., 1968. Transmission of tabacco rattle virus by Tri-chodorns species. Nemat%gica, 14: 20-24.

HOOF H. A. van, MAAT D. Z. and SEINHORST J. W., 1966. Viruses ofthe tabacco rattle virus group in Northem Italy: The vectorsand serological relationships. Neth.f. P/. path., 72: 253-258.

Hoy J. W., MIRCE11C S. M. and LoWNSBERY B. F., 1984. Differentialtransmission of prunus tornato ringspot virus strains by Xi-phinema ca/ifornicum. Phytopathology, 74: 332-335.

HUNT D. J., 1993. Aphe/enchidae, Longidoridae and Trichodori-dae: Their systernatics and bionomics. CAB Intemational, Wal-lingford, U. K., 352 pp.

JAIRAJPURI S. and AHMAD W., 1992. Dory/aimida Free-Living, Preda-ceous and P/ant-Parasitic Nematodes. New Delhi: Oxford andIBH Publishing Co. Pvt. Ltd.; Leiden: E. J. Brill, pp. 458.

JHA A. and POSNETTE A. F., 1959. Transmission of a virus to straw-berry plants by a nematode (Xiphinema sp.). Nature, 184:962-963.

JONES A. T., BROWN D. J. F., MCGAVIN W. J., RUDEL M. and ALTMAYAR

B., 1994. Properties of an unusual isolate of raspberry ring-spot virus from grapevine in Germany and evidence far itspossible transmission by Para/ongidorns maximus. Ann. app/.Bio/., 124: 283-300.

JONES A. T., MrrCHELL M. J. and BROWN D. J. F., 1989. Infectibility ofsome raspberry cultivars with arabis mosaic and raspberryringspot viruses and further evidence far variation in Britishisolates of these two viruses. Ann. app/. Bio/., 115: 57-69.

KLos E. J., FRONEK F., KNIERIM J. A. and CAll0N D., 1967. Peach ro-sette mosaic transmission and contrai. Quart. Bull. Mich. StateUnivo Agric. Exp. Sta., 49 287-293.

LAMBERTI F. and BLEVE-ZACHEO T., 1979. Studies on Xipbinemaamericanum sensu Iato with description of fifteen new spe-cies(Nematoda, Longidoridae). Nematol. medit., 7: 51-106.

LAMBER11 F. and CiANCIa A., 1993. Diversity of Xipbinema ameri-canum-group species and hierarchical cluster analysis of mor-phometrics. J. Nematol., 25: 332-343.

LEGORBORU F. J., 1993. Immunogenic structure of tabacco rattle vi-rus particles and its relation to vector transmission. Pb. D.Thesis. Univo Dundee, Scottando pp. 285.

llSTER R. M., 1964. Strawberry latent ringspot: a nematode-bomevirus. Ann. appl. Biol., 54: 167-176.

LooF P. A. A., 1975. Taxonomy of Trichodoridae, pp. 103-126. In:l'. Lamberti, C. E. Taylor and J. W. Seinhorst (Eds). NematodeVectors of PlanI Viruses. London. & New York: Plenum.

MARTELU G. P. and TAYLOR C. E., 1989. Distribution of viruses andtheir nematode vectors, Vol. 6, pp. 151-189. In: K. F. Harris(Ed.). Advances in Disease Vector Research. New York,

Springer-Verlag.McNAMARA D. G. and FLEGG J. J. M., 1981. The distribution of vi-

rus-vector nematodes in Great Britain in relation to rasi andpresent natural vegetation, pp. 225-235. In: J. M. Thresh (Ed.).Pests, Pathogens and Vegetation. London: Pitman.

MURANT A. F., 1983. Seed and pollen transmission of nematode-home viruses. Seed Sci. Tecbnol., 11: 973-987.

MURANT A. F., TAYLOR C. E. and CHAMBERS J., 1968. Properties, rela-tionships and transmission of a strain of raspberry ringspot vi-rus infecting raspberry cultivars immune to the common Scot-tish strain. Ann. appl. Biol., 61: 175-186.

NAVAS A., ANDRES M. FE. and ARiAS M., 1990. Biogeography of Lon-gidoridae in the Euromediterranea area. Nematol. medit., 18:103-112.

NAVAS A., BALDWIN J. G., BARRIOS L. and NOMBELA G., 1993. Phylog-eny and biogeography of Longidorus (Nematoda: Longidori-dae) in Euromediterranea. Nematol. medit., 21: 71-88.

NYLAND G., LoWNSBERY B. F., LoWE B. K. and MrrCHELL J. F., 1969.The transmission of cherry rasp leaf virus by Xipbinemaamericanum. Pbytopatbology, 59 1111-1112.

OSWALD J. W. and BoWMAN T., 1958. Studies on a soi!-bome potatovirus disease in Califomia. Pbytopatbology, 48: 396.

PLOEG A. T., BROWN D. J. F. and ROBINSON D. J., 1992. The associa-tion between species of Tricbodorns and Paratricbodorusvector nematodes and serotypes of tabacco rattle virus. Ann.appl. Biol., 121: 619-630.

PLOEG A. T., ROBINSON D. J. and BROWN D.J. F., 1993. RNA-2 of ta-bacco rattle virus encodes the determinants of transmissibi!ityby trichodorid vector nematodes. J. Cen. Virol., 74: 1463-1466.

RANA G. L. and ROCA F., 1973. Nematode transmission of artichokeltalian latent virus. 2nd Congr. internaz. Studi Carciofo, Bari,Italy, 21-24 nov. 1973, pp. 139-140.

ROBBINS R. T., 1993. Distribution of Xipbinema americanum andrelated species in North America. J. Nematol., 25: 344-348.

ROBBINS R. T. and BROWN D. J. F., 1991. Comments on the taxono-my, occurrence and distribution of Longidoridae (Nematoda)in North America. Nematologica, 37: 395-419.

ROBERTSON W. M. and HENRY C. E., 1986. An association of carba-hydrates with particles of arabis mosaic virus retained withinXipbinema dive~icaudatum. Ann. appl. Biol., 109 299-305.

ROCA F. and RANA G. L., 1981. Paratricbodorus tunisiensis (Nema-loda:. Trichodoridae). A new vector of tabacco rattle virus inltaly. Nematol. medit., 9 217-219.

ROCA F., RANA G. L. and KYRIAKOPOULOU P. E., 1982. Longidorusfasciatus Roca et lamberti vector of a serologically distinctstrain of artichoke Italian latent virus in Greece. Nematol.medit., lO; 53-69.

SALOMAO T. A., 1973. Soi! transmission ofartichoke yellow bandvirus. 2nd Congr. internaz. Studi Carciofo, Bari, Itaty, 21-24nov. 1973, pp. 831-854.

- 262 -

SANGER H. L., 1961. Untersuchungen uber schwer UbertragbarePorrnen des Rattlevirus. Proc. 4th Con! Potato Virus. Vis.,Braunschweig, Gennany, 1960, pp. 22-28.

S11JRHAND., 1984. Untersuchungen uber den Xiphinema coxi-com-plex (Nernatoda: Longidoridae). Nemat%gica 30; 305-323.

TAYLOR C. E., 1962. Transmission of raspbeny ringspot virus byLongidorns e/ongatus (De Man), (Nernatoda: Dorylaimoidea).Vir%gy, 17: 493-494.

TAYLOR C. E. and BROWN D. l. P., 1976. The geographical distribu-tion of Xiphinema and Longidorns in the British Isles and Ire-land. Ann. app/. Bio/., 84: 383-402.

TAYLOR C. E. and BROWN D. l. P., 1981. Nematode Virus Interac-tions, Vol. III, Chap. Il, pp. 281-301. In: B. M. Zuckerrnanamd R. A. Rhodes (Eds) Plant Parasitic Nernatodes. New York:Academic Presso

TAYLOR C. E., BROWN D. l. P., NEIISON R. and loNEs A. T., 1994. Thepersistence and spread of Xiphinema diversicaudatum (Nem-atoda: Dorylaimida) in cultivated and uncultivated biotopes.Ann. app/. Bio/., 124: 469-477.

TAYLOR C. E. ROBERTSON W. M., 1969. The location of raspbenyringspot and tornato black ring viruses in the nematode vec-tor, Longidorus e/ongatus. Ann. app/. Bio/., 64: 233-237.

TAYLOR C. E. and ROBERTSON W. M., 1970a. Sites of virus retentionin the alimentary tract of the nematode vectors, Xipbinemadiversicaudatum (Micol.) and X. index (Thorne and Allen).Ann. app/. Bio/., 66 375-380.

TAYLOR C. E. and ROBERTSON W. M., 1970b. Location of tabacco rat-tle virus in the nematode vector Tricbodorns pacbydennusSeinhorst. J. Gen. Viro/., 6 179-182.

TAYLOR C. E. and THOMAS P. R., 1968. The association of Xpbine-ma diversicaudatum (Micoletzky) with strawberry latent ring-spot and arabis mosaic viruses in a raspberry plantation. Ann.app/. Bio/., 62: 147-157.

TOPHAM P. B. and ALPHEY T. J. W., 1985. Faunisticanalysis of lon-gidorid nematodes in Europe. J. Biogeog., 12: 165-174.

VRAIN T. C., 1993. Restriction fragment length polymorphism sep-arates species of me Xipbienma americanum group. J. Nema-to/., 25: 361-366.

WALKINSHAW C. H., GRIFFIN G. D. and LARSON R. H., 1961. Tricbod-orus cbrutiei as a vector of potato corky ringspot (tobaccorattle) virus. Pbytopatb%gy, 51: 806-808.

YAGrrA H. and KOMURO Y., 1972. [Transmission of mulberry ring-spot virus by Longidorus marlini Merny]. Ann. Pbytopatb.Soc.Japan, 38: 275-283.

Accepted for publication on 2 September 1994.

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