There is a core of nematode species that are targeted by legislation around the world.
Of course, not all species of plant-parasitic nematodes appear on every country’s list of regulated pests because they may be endemic in some countries or regions and exotic in others. A list of plant-parasitic nematodes most frequently regulated in international trade over three decades is given in Table 12.1. Plant-parasitic nema- todes, with their endoparasitic, sedentary and migratory habits, are a major target of phytosanitary measures because they can be easily transported unseen via roots, soil and above-ground parts of plants. The pinewood nematode B. xylophilus, a major forestry pest in some parts of the world that has also been introduced into two EU countries, Portugal (Mota et al., 1999) and Spain (Robertson et al., 2011), can be either mycetophagous or ectoparasitic and is spread by infested timber and timber products or by beetle vectors on a local scale. As this species has spread, it has been regulated by an increasing number of countries.
Reasons for the spread of other species over the years are a matter of speculation.
In some instances, the significance of spread by uncertified potato tubers, bare-rooted plants for planting and excessive soil residues has been recognized, leading to addi- tional regulation. However, the new appearance of Longidorus diadecturus in 2011 data, included in Table 12.1, appears to be a result of the expanding membership of the
Table 12.1. Number of countries regulating species of plant-parasitic nematode in 1982, 2000 and 2011.1
Nematode species 1982 2000 2011
Globodera rostochiensis 51 106 119
Bursaphelenchus xylophilus –* 46 82
Globodera pallida –* 55 80
Ditylenchus dipsaci 23 58 72
Ditylenchus destructor 12 53 65
Radopholus similis2 11 55 58
Heterodera glycines –* 52 55
Aphelenchoides besseyi 9† 70 54
Meloidogyne chitwoodi –* –* 52
Nacobbus aberrans –* 38 52
Xiphinema americanum –* 30 43
Xiphinema californicum –* –* 39
Meloidogyne fallax –* –* 39
Longidorus diadecturus –* –* 33
Pratylenchus penetrans –* –* 25
Aphelenchoides fragariae 13 47 21
Anguina tritici –* 24 21
Bursaphelenchus cocophilus –* 21 13
Heterodera schachtii 16 22 14
Xiphinema index –* 42 6†
1Data for species regulated in more than ten countries as recorded by Kahn (1982), Lehman (2004), Hockland et al. (2006) and the APHIS/USDA Phytosanitary Certificate Issuance and Tracking System (PCIT) (2011). Countries belonging to the EU were regarded as individual countries.
22011 data for Radopholus similis includes countries regulating R. citrophilus, which has been proposed as a species in its own right but is now variously accepted as a subspecies or race of R. similis.
In 2011, 11 countries listed only R. similis in their regulations, two countries listed only R. citrophilus and 45 countries listed both.
* Insufficient or no records at this time.
†Species regulated by fewer than ten countries but included here to show changes between 1982 and 2011. Since 2004, L. diadecturus, M. chitwoodi and M. fallax were regulated by more than ten countries. In 2011, the combination of B. cocophilus and its weevil vector, Rhynchophorus palmarum, was regulated by more than 35 countries.
EU and other countries adopting the official EU list, rather than an increased risk in the spread or significance of this pest. At the time of the first EU list of quarantine nema- todes, this species was thought to transmit viruses in its type country, USA, and was thus included. Recent data in Table 12.1 showing a significant decrease in importance of some species may be due to increased survey work showing the previously unknown distribution of some species, or establishment of some species in new areas. Xiphinema index remains an important regulated pest in California and Florida; H. schachtii, widespread in Europe, which contributes almost 50% to world sugar beet production, has been the subject of intensive, rigorous control measures that include new resistant cultivars, but it remains a significant regulated pest in South America and parts of Asia.
Nematode pests of potatoes are amongst the most highly regulated because they are readily spread in infested tubers or associated soil residues and because potatoes destined for consumption may instead be propagated. PCN species are in the top three nematodes listed in Table 12.1. Other than PCNs, H. glycines is the only
cyst-forming nematode commonly regulated by countries. It is of major concern for several countries in North America (Canada), South America (e.g. Argentina, Brazil, Chile, Uruguay) and African countries such as South Africa. This nematode is of less concern in the Far East where it is native. The false root-knot nematode, Nacobbus aberrans, another major potato pest, is included on the list of regulated pests for many countries including Brazil, Japan, Korea, Paraguay and the EU. This nematode has not yet received the same level of concern as PCN species, although it has the potential to infest a wider range of crops (Manzanilla-López et al., 2002).
In general, root-knot nematodes are not regulated as a group because the major economically important species are already widely distributed. However, several spe- cies emerging from Africa and the Americas are now causing concern. Table 12.1 includes two root-knot nematodes for the first time in this edition. Meloidogyne chitwoodi is included primarily because it is a serious pest of potato and other eco- nomically important crops such as carrot. It is on the lists of prohibited pests of many countries (Canada, the EU, Mexico, and other countries in Latin America and the Far East). Meloidogyne fallax, another pest of potato, is also now recognized as an important pest by many countries. Other root-knot nematodes are being included on
‘alert’ lists worldwide: M. citri, a pest of citrus in China which was thought to have a restricted host range but has now been shown to infest and reproduce on hosts such as tomato (Vovlas and Inserra, 2000); M. ethiopica, a very damaging pest of kiwi and grape in Brazil and Chile, respectively, recently introduced into Europe (Sˇircaet al., 2004);M. enterolobii (= M. mayaguensis), which has been shown to overcome root- knot nematode resistant genes in some economically important crops (Brito et al., 2007; Kiewnick et al., 2009) and has been added to the EPPO Alert List A2 as recom- mended for regulation as a quarantine pest.
Because endoparasitic nematodes are found within plant parts, they can easily be moved in infested plant material in trade. Migratory endoparasitic nematodes, such as the burrowing nematode, Radopholus similis, are common in lists of quarantine pests. The occurrence of a R. similis race able to infest and damage citrus in Florida and the lack of reliable and rapid morphological and molecular analyses to identify this race has prompted a worldwide ban against this nematode, especially in citrus- growing countries. More than 50 countries regulate this nematode, which is consid- ered the most damaging nematode pest of citrus. The risk from introducing other damaging citrus nematode pests is believed to be sufficiently reduced by measures in place for R. similis, such that further restrictions are not deemed necessary by many countries. Specific restrictions against other endoparasitic migratory root feeders are imposed by Argentina, Brazil, Chile, Egypt, Mexico, Morocco, South Africa, Syria and Uruguay but the risk associated with these nematodes is considered less serious than that posed by R. similis. Listed root-lesion nematode pests include mainly tropi- cal and subtropical species such as Pratylenchus coffeae, P. loosi, P. scribneri and P. zeae and the temperate species P. penetrans; the latter is a new entrant in Table 12.1 for 2011.
Migratory endoparasitic species of foliar parts of plants are regulated by many countries; species belonging to the genera Aphelenchoides and Ditylenchus are most common in quarantine lists. Their frequent inclusion in the majority of the lists is due to the fact that these nematodes are easily transported inside plant tissues. These nematodes may cause symptoms that can be detected by visual inspection by well- trained inspectors, but at low levels such symptoms may not be apparent (Kohl et al.,
2010). Often the appearance of plants may also suggest nutritional disorders and so laboratory confirmation is necessary. The insect-vectored species such as B. xylophilus andB. cocophilus, which also live inside foliar parts of plants, are also of major con- cern for many countries.
Ectoparasitic nematodes are found in the soil surrounding plant roots, rather than within plant material, so restrictions on the amount of soil associated with plants and plant products will reduce the risk of their introduction (nil tolerance or a few derogations internationally), so that these nematodes are less likely to follow trade pathways and hence they are rarely included in regulated pest lists. However, ectoparasitic nematodes that vector nepoviruses (dagger and needle nematodes) are of major concern for European and a few South American countries (e.g. Brazil and Uruguay). Nematodes in the Xiphinema americanum sensu lato species complex are among the most commonly regulated ectoparasitic species, as the overall risk of intro- duction of virus vectors in this group is considered higher than that of many other damaging ectoparasitic nematodes such as lance (Hoplolaimus spp.) and sting nema- todes (Belonolaimus spp.), even though the pathway of introduction of all these spe- cies poses the same potential risk. Further details of nematodes listed by countries around the world can be obtained from the EPPO Plant Quarantine Data Retrieval (PQR) System, details of which can be found on the EPPO website (http://www.eppo.
int), or the IPPC website (http://www.ippc.int).