Decraemer, Wilfrida

Robbins, Rob

English

Ghent University Academic Bibliography

The Who, What and Where of Longidoridae and TrichodoridaeWilfrida Decraemer,1 R. T. Robbins2WHO: LONGIDORIDAE AND TRICHODORIDAELongidoridae and Trichodoridae represent the onlyfamilies of nematodes within the Class Enoplea provento be plant-parasitic. The Longidoridae are classifiedwithin the subclass Dorylaimia (order Dorylaimida, su-perfamily Dorylaimoidea), while the Trichodoridae be-long to the subclass Enoplia (order Triplonchida, su-perfamily Diphtherophoroidea).Longidoridae: The family Longidoridae includes some480 species of the subfamily Longidorinae with six gen-era: Longidorus (144 spp.), Longidoroides (13 spp.) andParalongidorus (72 spp.) in the tribe Longidorini, andAustralodorus (1 sp.), Paraxiphidorus (3 spp.) and Xiphi-dorus (8 spp.) in the tribe Xiphidorini and the subfam-ily Xiphineminae with one genus Xiphinema (some 240spp.). At present, there is no consensus about the statusof the genus Longidoroides Khan, Chawla and Saha, 1978(see Decraemer and Coomans, 2007). Longidorus, Para-longidorus and Xiphinema are virus vectors. A wealth ofinformation on Longidorus, Paralongidorus and Xiphi-nema can the found in papers on polytomous keys andsubsequent supplements: Xiphinema (Loof and Luc,1990; Loof and Luc, 1993; Loof et al., 1996), Longidorus(Chen et al., 1997; Loof and Chen, 1999) and Para-longidorus (Escuer and Arias, 1997) as well as in Coo-mans et al. (2001), a monography on the genus Xiphi-nema dealing with character analysis, phylogeny andbiogeography.The main diagnostic features of Longidoridae at thegenus level are the structure of the odontostyle andodontophore, the structure and position of the guidering, the shape of the amphidial fovea, shape and sizeof amphid opening and the position and size of thepharyngeal gland nuclei. Additional features at specieslevel next to morphometric data are the shape and sizeof the amphidial fovea and opening, the developmentand structure of the female reproductive system (didel-phic, monodelphic, pseudomonodelphic) with uterinedifferentiation and inclusions in Xiphinema and generaof the Xiphidorini, the tail shape in all developmentalstages and presence or absence of males. Phylogeneticanalyses of the Longidoridae based on sequence dataand morphological data were carried out by He et al.(2003). Olivera and Neilson (2004) have a comprehen-sive review article showing the systematics, virus vector-ing species and morphological differences among theLongidorid genera, and Decraemer and Coomans(2007) discussed relationships within the familyLongidoridae.Trichodoridae: The Trichodoridae include 100 speciesand five genera: Trichodorus Cobb, 1913, ParatrichodorusSiddiqi, 1974, Monotrichodorus Andrassy, 1976, Allotri-chodorus Rodriguez-M, Sher and Siddiqi, 1978 andEcuadorus Siddiqi, 2002. The two largest genera Tricho-dorus (54 spp.) and Paratrichodorus (34 spp.) are didel-phic in females and occur worldwide. The three re-maining genera, Monotrichodorus (4 spp., one subspe-cies), Allotrichodorus (6 spp.) and Ecuadorus (2 spp.),have fewer species, and females are monodelphic-prodelphic; so far, these three genera have only beenrecorded from Central America and the northern partof South America.The main diagnostic characters to differentiate thegenera of the Trichodoridae are: in females, (i) thereproductive system (didelphic or monodelphic); (ii)length of vagina, (iii) development of vaginal sclero-tized pieces and (iv) presence of advulvar lateral bodypores; and in males, (i) presence or absence of caudalalae, (ii) degree of development of copulatory musclesand related habitus and (iii) development of capsule ofspicule suspensor muscles (Decraemer and Geraert,2006). Additional features at species level, apart frommorphometric data, are: in females, (i) the vaginal scle-rotized pieces (size, shape, orientation, distance), (ii)presence/absence and location of sperm cells; in malesand females, structure of sperm cell and nucleus, andin males, (i) the spicules (shape, ornamentation), (ii)number and arrangement of ventromedian cervical pa-pillae and (iii) ventromedian precloacal supplements.Decraemer (1995) gives a comprehensive review ofmorphological and systematic information on thisgroup.WHAT: VIRUS VECTORSThe Longidoridae and Trichodoridae are polypha-gous root-ectoparasites and are the only plant-parasiticNematoda that transmit plant viruses. Their associatedviruses belong to different virus taxa. Longidorids vec-tor nepoviruses; whereas trichodorids vector Tobravi-ruses (Taylor and Brown, 1997).Longidoridae: Of the 38 known nepoviruses, 13 havebeen proven to be naturally transmitted by Longi-doridae: seven by Longidorus species, one by Paralongi-dorus and nine by Xiphinema species. Thus, only 5% ofthe known species of Longidoridae have been shown totransmit nepoviruses. The North American Xiphinemaspecies, and more specifically the X. americanum speciesgroup, seems to present the main source of virus vec-Received for publication November 20, 2007.1 Royal Belgian Institute of Natural Sciences, Brussels, Belgium.2 University of Arkansas, Fayetteville, AR.A paper given at the symposium on Systematics and Phylogeny: “The Tree ofLife, Dorylaimina, Triplonchida and the Origin of Nematodes” at the jointmeeting of APS and SON at San Diego, CA, July 28-August1, 2007.E-mail: rrobbin@uark.eduThis paper was edited by David Bird.Journal of Nematology 39(4):295–297. 2007.© The Society of Nematologists 2007.295toring, i.e., three vector species of the X. non-ameri-canum-group (X. index, X. diversicaudatum, X. italiae) vs.six putative species of the X. americanum group (X.americanum s.str., X. californicum, X. bricolense, X. interme-dium, X. revesi, X. tarjanense). In North America, thefour nepoviruses cherry rasp leaf, peach rosette mosaic,tobacco ringspot and tomato ringspot are transmittedby members of the Xiphinema americanum group of spe-cies. These viruses cause substantial damage to a widerange of fruit and vegetable crops (Taylor and Brown,1997).Trichodoridae: All tobraviruses are transmitted bytrichodorid vector species. Only the didelphic tricho-dorid genera possess virus vector species. Out of 54Trichodorus and 34 Paratrichodorus species, 7% (four: T.primitivus, T. similis, T. cylindricus and T. viruliferus) and26% (nine: P. anemones, P. divergens, P. hispanus, P. na-nus, P. pachydermus, P. teres, P. tunisiensis, P. allius, P.minor, P. porosus) are vectors of tobraviruses, respec-tively. For Europe, however, the percentages of virusvectors vs. non-vectors are much greater; 67% for Para-trichodorus and 27% for Trichodorus. Further, in nearlyall European countries, vector species and virus arepresent (Ploeg and Decraemer, 1996). This supportsthe hypothesis that Trichodorus vector/virus associationprobably evolved in Europe. The presence of these vec-tor species in North America is very restricted and ap-parently the result of introduction with imported plantmaterial. Similar remarks can be made for P. pachyder-mus, P. anemones, P. teres, P. divergens, P. hispanus, P.nanus and P. tunisiensis, all species whose main occur-rence is restricted to Europe and Mediterranean coun-tries. For P. porosus, the vector aspect is based on labo-ratory experiments. The vector species P. allius and P.minor apparently developed a virus/vector relationshipoutside Europe and, with P. minor, possess a uniqueassociation with pepper ringspot virus (PPV) restrictedto Brazil, South America.WHERE: DISTRIBUTIONLongidoridae: Among the genera of Longidoridae,some are considered cosmopolitan, while others havevery limited distribution (Coomans 1995). Longidorusand Xiphinema are taxa with examples found in all in-habited continents. Australodorus, Paraxiphidorus and Xi-phidorus are quite limited in distribution, i.e., onlySouth America.The genus Longidorus has been found most fre-quently in Europe (73 spp.), followed by India (25spp.), North America (23 spp.), South Africa (18 spp.)and China (13 spp.). In South America, two specieshave been reported, and in Australia and New Zealandfour species. Three North American species have beenshown to be serious pests on certain crops in sandysoils, L. breviannulatus in the mid-west on corn (Zeamays), L. africanus on several crops in southern Califor-nia and L. americanum on loblolly pine in Georgia.The genus Paralongidorus (incl. Longidoroides) hasbeen reported mainly from India (34 spp.) and SouthAfrica (29 spp.). In Europe, nine species have beenrecorded, and three from Australia. In the Americas,only two species have been reported, both in NorthAmerica. Ninety percent of the Paralongidorus specieswere recorded only once or, if several times, then fromwithin a restricted area, 5% from two continents, andno cosmopolitan species has been found.The genus Longidoroides has been reported mainly inIndia and South Africa. The range of the genera Aus-tralodorus, Paraxiphidorus and Xiphidorus is limited toSouth America, with Xiphidorus being the most widelydistributed (Argentina, Brazil, Uruguay and Venezu-ela).The genus Xiphinema is the most diversified genus ofthe family Longidoridae with both species groups, theX. americanum-group and the non-americanum-group, oc-curring worldwide. Lamberti et al. (2000) gave an over-view of the geographic distribution of the X. america-num-group. A nearly equal number of species has beenreported from North America (21) and Asia (22), fol-lowed by 17 for Europe, 11 for South America, 10 forAfrica and three for Australia. However, 50% or moreof the species are considered rare species or of ques-tionable identification. The largest number of commonspecies is found in North America (10) and Europe (8).The biogeographic distribution of the Xiphinema non-americanum species group was studied in detail in Coo-mans et al. (2001). The authors divided the species intofour groups: (1) species recorded only once or, whenrecorded more, only from a restricted area, (2) speciesrecorded in different areas but close to each other orbelonging to the same climatic unit, (3) species foundin two continents and (4) ‘cosmopolitan’ species fromat least three different continents. Xiphinema speciesappeared far more numerous in tropical areas com-pared to temperate ones. Sixty-five percent of the X.non-americanum group belong to group 1, with the high-est diversity recorded from Southeast Africa (53 spp.)and Europe (33 spp.). Only 16% of the species belongto group 2; 8% were recorded from two continents and10% appear as putative cosmopolitan species. The highnumber of species recorded from Portugal (19 spp.)and South Africa (40 spp.) might be the result of evo-lutionary radiation as well as high taxonomic activity.Trichodoridae: The genus Trichodorus is a cosmopoli-tan genus but predominant in the more temperate re-gions. Trichodorus is widespread in Europe and NorthAmerica, respectively, with 17 and 20 species recorded.In South Africa, nine species have been recorded, allbut one from natural vegetation and all being consid-ered endemic for this region. A similarly high numberof species has been recorded from China, but only twospecies are restricted to this vast country. Former datamay be biased by differences in the extension and num-ber of surveys, e.g., we have to take into account that296 Journal of Nematology, Volume 39, No. 4, December 2007Europe, North America and South Africa are also themost extensively surveyed regions with more easily as-sessable published data and reports. Further, the rec-ords have to be interpreted with caution because of theresults of anthropogenic impact. In Europe, 15 of the17 species seems to be endemic, while for NorthAmerica only seven species have been restricted to thiscontinent; a large number of the American records arerare records of introduced European species, the mostwidely distributed one being T. primitivus. Currently, noTrichodorus species have been recorded from Australiadespite national surveys from crop plants and nativevegetation. Only one-fifth of the species appears to oc-cur in former Gondwanaland countries. From this, itcan be assumed that the genus probably originated inLaurasia, with the main center of speciation in Europe.The genus Paratrichodorus is also a cosmopolitan ge-nus but mainly present in tropical and subtropical re-gions. About 75% of Paratrichodorus species have beendescribed from former Gondwanaland. This is nicelyillustrated by the current distribution for example of P.lobatus and P. porosus. Paratrichodorus minor is the mostwidely distributed Paratrichodorus species, present inmost of the surveyed countries in Africa and recordedin Australia, but also in South America, CentralAmerica, the West Indies and southern regions ofNorth America.So far, the monodelphic genera, Monotrichodorus, Al-lotrichodorus and recently Ecuadorus, have been de-scribed only from the Neotropical region, with Mono-trichodorus being widely recorded to the north andnorth west of the Amazon Basin (except for M. proporifer(= M. m. monohystera) from Para State, Brazil), Allotri-chodorus only from the southeast of the Basin and re-stricted to Bahia State and Ecuadorus from Trinidad,Bahia State, Brazil, Martinique and Ecuador. Most ofthese species have been found associated with naturalvegetation next to agricultural corps. Their associationwith native plants supports the theory that the mono-delphic trichodorids are endemic to tropical South andCentral America. Ecuadorus, only known by partheno-genetic females, occupies a somewhat intermediate po-sition between monodelphic (Allotrichodorus) and didel-phic (Paratrichodorus) genera in morphological featuresand distribution. Prior to the introduction of the genusEcuadorus by Siddiqi (2002), the type species E. westin-dicus had been classified first within the genus Para-trichodorus, later within Allotrichodorus and was consid-ered Allotrichodorus westindicus a species incertae sedis inHunt (1993).The discovery of three neotropical genera, Mono-trichodorus, Allotrichodorus and Ecuadorus, has clearlydemonstrated that parallel evolution in the characternumber of genital branches in the female reproductivesystem and corresponding presence/absence of bursain males (few exceptions) has occurred in the vicariat-ing didelphic and monodelphic genera. Different fromthe Longidoridae, no separate tribes have been as-signed.The existence of a transformation series from P. mi-nor, P. caribbensis to Ecuadorus westindicus supports thehypothesis that the monodelphic genera have devel-oped from an ancestral stock just before or after thesplitting off of current South America in the Cretaceousperiod.LITERATURE CITEDChen, Q.-W., Hooper, D., Loof, P. A. A., and Xu, J. 1997. A revisedpolytomous key for the identification of species of the genusLongidorus Micoletzky, 1922 (Nematoda: Dorylaimoidea). Fundamen-tal and applied Nematology 20:15–28.Coomans, A. 1996. Phylogeny of the Longidoridae. Russian Journalof Nematology 4:51–60.Coomans, A., Huys, R., Heyns, J., and Luc, M. 2001. Characteranalysis, phylogeny, and biogeography of the genus Xiphinema Cobb,1973 (Nematoda, Longidoridae). Annales du Musée Royal del’Afrique Centrale (Zoologie), Tervuren, Belgique 287:1–239.Decraemer, W. 1995. The Family Trichodoridae: Stubby Root andVirus Vector Nematodes. Developments in Plant Pathology, 6. Dor-drecht: Kluwer Academic Publishers.Decraemer, W., and Coomans, A. 2007. Revision of some species ofthe genus Paralongidorus sensu Siddiqi et al. (1993) with a discussionon the relationships within the family Longidoridae (Nematoda:Longidoridae). Nematology 9:643–662.Decraemer, W., and Geraert, E. 2006. Ectoparasites. Pp. 153–184 inR. Perry and M. Moens, eds. Plant Nematology Wallingford, UK:CABI publishing.Escuer, M., and Arias, M. 1997. Paralongidorus iberis and P. monegren-sis sp.n. from Hooper & Khan, 1963 (Nematoda: Longidoridae). Fun-damental and Applied Nematology 20:135–148.He, Y., Li, H., Brown, D. J. F., Lamberti, F., and Moens, M. 2003.Isolation and characterization of microsatellites for Xiphinema indexusing degenerate oligonucleotide primed PCR. Nematology 5:809–819.Hunt, D. J. 1993. Aphelenchida, Longidoridae and Trichodoridae:Their Systematics and Bionomics. Wallingford, UK: CABI Publishing.Lamberti, F., Molinari, S., Moens, M. and Brown, D. J. F. 2000. TheXiphinema americanum group. I. Putative species, their geographicaloccurrence and distribution, and regional polytomous identificationkeys for the group. Russian Journal of Nematology 8:65–84.Loof, P. A. A., and Chen, Q. 1999. A revised polytomous key for theidentification of species of the genus Longidorus Micoletzky, 1922(Nematoda: Dorylaimoidea). Supplement 1. Nematology 1:55–59.Loof, P. A. A., and Luc, M. 1990. A revised polytomous key for theidentification of species of the genus Xiphinema Cobb, 1913 (Nema-toda: Longidoridae) with exclusion of the X. americanum-group. Sys-tematic Parasitology 16:35–66.Loof, P. A. A., and Luc, M. 1993. A revised polytomous key for theidentification of species of the genus Xiphinema Cobb, 1913 (Nema-toda: Longidoridae) with exclusion of the X. americanum-group:Supplement 1. Systematic Parasitology 24:185–189.Loof, P. A. A., Luc, M., and Baujard, P. 1996. A revised polytomouskey for the identification of species of the genus Xiphinema Cobb,1913 (Nematoda: Longidoridae) with exclusion of the X. americanum-group: Supplement 2. Systematic Parasitology 33:23–29.Oliveira, M., Hübschen, J., Brown, D. J. F., Ferraz, L. C. C. B.,Wright, F., and Neilson, R. 2004. Phylogenetic relationships amongXiphinema and Xiphidorus nematode species from Brazil inferred from18S rDNA sequences. Journal of Nematology 36:153–159.Ploeg, A., and Decraemer, W. 1996. The occurrence and distribu-tion of trichodorid nematodes and their associated tobraviruses inEurope and the former Soviet Union. Nematologica 43:228–251.Siddiqi, M. R. 2002. Ecuadorus equatorius gen. n., sp. n. and Na-nidorus mexicanus sp. n. (Nematoda: Trichodoridae). InternationalJournal of Nematology 12:197–202Taylor, C., and Brown, D. 1997. Nematode Vectors of Plant Viruses.Wallingford, UK: CABI.Longidoridae and Trichodoridae: Decraemer and Robbins 297

The Who, What and Where of Longidoridae and Trichodoridae

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The Who, What and Where of Longidoridae and Trichodoridae

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