1 Distribution and economic importance K.Evansandf.A.Rowe

1.1 INTRODUCTION The family of plant parasitic contains the cyst• forming species within the sub-family , within which the numbers of genera (not all cyst-forming) and species described have increased greatly over the last five decades. When Franklin (1951) pub• lished her book on "The cyst-forming species of ", cyst nema• todes were already a major concern and were known to cause serious yield lasses in important food crops such as potatoes, cereals, brassicas, tomatoes and sugar beet. The genus Heterodera Schmidt 1871 was, at that time, considered tobe largely temperate, with about 12 species. Today, 67 valid species are recognized in the genus Heterodera alone (Table 1.1). After many studies and revisions in classification (Mulvey, 1972; Stone, 1977; Luc, Maggenti and Fortuner, 1988; Baldwin and Schauest, 1990), the specific characters of many other species that were once members of the genus Heterodera have been accommodated in new genera. These new genera of cyst-forming species are Globodera, Punctodera, Cactodera, Afe• nestrata and Dolichodera, which are listed with the species they contain in Table 1.2. The cyst-forming genera of the Heteroderinae seem, in general, to have hosts within particular plant families. For instance, the support many species of Heterodera and Punctodera. On the other hand, there are examples of unusual host specificity within genera, such as Cactodera betulae, found normally on birch and occasionally alder whilst other species of Cactodera are found on members of the Cactaceae, Amar• anthaceae and Chenopodiaceae.

The Cyst Nematodes. Edited by S.B. Sharrna. Published in 1998 by Chaprnan & Hall, London. ISBN 0 412 75530 0. 2 Distribution and economic importance Table 1.1 Cyst-forming species of the genus Heterodera Schmidt, 1871

Species Main host plant family Species Main host plant family amygdali Rosaceae limonii Plumbaginaceae arenaria Poaceae litoralis Chenopodiaceae aucklandica Poaceae longicolla Poaceae avenae Poaceae mani Poaceae bergeniae Saxifragaceae medicaginis Fabaceae bifenestra Poaceae mediterranea Anarcardiaceae cajani Fabaceae menthae Lamiaceae canadensis Cyperaceae methwoldensis not known cardiolata Poaceae mothi Cyperaceae carotae Umbelliferae oryzae Poaceae ciceri Fabaceae oryzicola Poaceae cruciferae Cruciferae oxiana Chenopodiaceae cynodontis Poaceae pakistanensis Poaceae cyperi Cyperaceae phragmitidis Poaceae daverti Fabaceae plantaginis Plantaginaceae delvii Poaceae polygoni Polygonaceae elachista Poaceae raskii Cyperaceae fici Moraceae rosii Polygonaceae filipjevi Poaceae sacchari Poaceae galeopsidis Lamiaceae salixophila Salicaceae gambiensis Poaceae schachtii* Chenopodiaceae glycines Fabaceae sinensis Poaceae glycyrrhizae Fabaceae sonchophila Asteraceae goettingiana Fabaceae sorghi Poaceae graduni Polygonaceae spinicaudata Poaceae graminis Poaceae tadshikistanica Asteraceae graminophila Poaceae trifolii Fabaceae hordecalis Poaceae turangae Salicaceae humuli Moraceae turcomanica Chenopodiaceae iri Poaceae urticae Urticaceae kirjanovae Betulaceae ustinovi Poaceae latipons Poaceae uzbekistanica Salicaceae lespedezae Fabaceae zeae Poaceae leuceilyma Poaceae

* Type species Note: Many species of Heterodera will parasitise plants of more than one family, notably the type species H. schachtii. The main host plant family given is generally the most important host family but, occasionally, the family with which the species was first associated.

1.2 DISTRIBUTION It is now known that, far from being exclusively temperate, many cyst nematodes (and also non-cyst-forming species of the Heteroderinae) are present in tropical and sub-tropical regions. The numbers of known Distribution 3

Table 1.2 Cyst-forming species of genera other than Heterodera

Genus Authority Species Hast plant family Afenestrata (5) Baldwin and Bell, 1985 africana* Poaceae axonopi Poaceae koreana Poaceae orientalis not known sacchari Poaceae Cactodera (11) Krall and Krall, 1978 acnidae Amaranthaceae amaranthi Amaranthaceae aquatica not known betulae Betulaceae cacti* Cactaceae chaubattia Rosaceae estonica Polygonaceae eremica Chenopodiaceae milleri Chenopodiaceae thornei Portulaceae weissi Polygonaceae Dolichodera (1) Mulvey and Ebsary, fluvialis* Poaceae 1980 (unconfirmed) Globodera (12) Skarbilovich, 1959 achilleae Asteraceae artemisiae Asteraceae hypolysi Asteraceae leptonepia unknown, possibly Solanaceae millefolii Asteraceae (sp. inq.) mirabilis unknown (sp. inq.) pallida Solanaceae rostochiensis* Solanaceae tabacum Solanaceae solanacearum tabacum Solanaceae tabacum tabacum Solanaceae virginiae zelandica Onagraceae chalcoensis Poaceae Punctodera (3) Mulvey and Stone, matadorensis Poaceae 1976 punctata* Poaceae

* Type species 4 Distribution and economic importance species increase as awareness of the darnage they cause is observed and taken into account by farmers, agricultural advisers and, eventually, nematologists. The genus Afenestrata was first described by Baldwin and Bell (1985) after close re-examination of Sarisodera africana; the num• ber of species has now risen to five. The genus Globodera is thought to have originated in the Andean regions of South America (Krall and Krall, 1978), and divides geographically into two main groups, the G. tabacum group of species from North America and the potato cyst nematodes (G. pallida and G. rostochiensis) from South America. Although Globodera is considered to have evolved in the Americas, mainly on members of the Solanaceae, there is a small group of Globodera species from the Old World which parasitize members of the Asteraceae, and G. zealandica is a species indigenous to New Zealand whose hosts are woody trees from the Onagraceae (Wouts, 1984). The species parasitizing the Asteraceae may represent a group that have co-evolved with their hosts in an isolated evolutionary niche after the splitting of Gondwanaland (Stone, 1983), and they are distributed in Europe, the former USSR, China and Japan. It is of note that they may be able to survive in extreme climatic conditions. The most economically important species of the cyst-forming nematodes are within the genera Heterodera and Globodera. The non• cyst-forming genera of the Heteroderinae are listed in Table 1.3. The most important cyst-forming genera, Heterodera, Globodera and Punctodera,

Table 1.3 Non-cyst forming genera within the sub-family Heteroderinae

Number of Genus Authority species Atalodera Wouts and Sher, 1971 4 Bellodern Wouts, 1985 1 Bilobodera Sharma and Siddiqi, 1992 2 Brevicephalodera Kaushal and Swarup, 1989 1 Camelodera Krall, Shagalina and Ivanova, 1988 1 Cryphodera Colbran, 1966 5 Ekphymatodera Baldwin, Bernard and Mundo-Ocampo, 1 1989 Hylonema Luc, Taylor and Cadet, 1978 1 Meloidodera Chitwood, Hannon and Esser, 1956 9 Rhizonema Cid del Prado Vera, Lownsbery and 1 Maggenti, 1983 Sarisodera Wouts and Sher, 1971 1 Thecavermiculatus Robbins, 1978 4 Verutus Esser, 1981 2 + 1 undescribed Heterodera 5 important cyst-forming genera, Heterodera, Globodera and Punotcdera are considered separately below and the non-cyst-forming genera within the Heteroderinae are considered briefly as a group.

1.2.1 Heterodera Members of the genus Heterodera are believed originally to have para• sitized ancient orders of tropical plants and to have evolved to the present time on those members of the plant families that may stillexist (Krall and Krall, 1978). For convenience, the members of the genus Heterodera are considered here under the headings Tropical, Sub-tropical and Temperate, but it must be recognized that there is considerable overlap between these empirical groupings.

(a) Tropical In the tropics, at least 23 species of cyst have been found (Table 1.4), plus other non-cyst-forming genera of the Heteroderidae such as Bilobodera (Sharma and Siddiqi, 1992), Brevicephalodera (Kaushal and Swarup, 1989) and Hylonema (Luc, Taylor and Cadet, 1978). As far as is known, the cyst-forming species are more damaging than non-cyst-form• ing species and, according to Luc (1986), the most economically-import• ant in the tropics are H. oryzae, H. sacchari, H. oryzicola, H. cajani and H. zeae, to which we add H. sorghi. and H. oryzicola both attack the staple crops and bananas. The type locality for H. oryzae is the Ivory Coast on rice and it is found in Senegal, parasitising banana. It has been recorded by Shahina and Maqbool (1995) from Pakistan and by Chinnasri, Tangchitsamkid and Toida (1994) from Thailand. is present in Goa, Haryana and Kerala in India on upland rice, and on banana (Musa acuminata x M. balbisiana) and (Charles and Venkitesan, 1978; Rao and Jayaprakash, 1978). is morphologically very similar to H. oryzae with some overlap in morphometric values. Although H. sacchari was origin• ally reported from sugar cane in the Congo, it has also been reported on sugar cane from other countries such as Nigeria (Jerath, 1968; Odihirin, 1975) and Pakistan (Maqbool, 1981), and from in India (Swarup, Prasad and Raski, 1964). It has also been reported as a parasite of rice (Merny, 1970; Babatola, 1983) and its distribution may even extend to Jamaica where it was reported in soil around sugar cane roots, although only second stagejuveniles were found (Singh, 1974). The other cyst nematode known to cause darnage to rice, H. elachista, has so far only been recorded from upland rice in Japan (Ohshima, 1974) and appears to be very different from the three Heterodera 6 Distribution and economic importance

Table 1.4 Cyst nematodes from the hot tropics

Species Host(s) Distribution

Afenestrata Panicum maximum Ivory Coast africana Cactodera Amaranthus viridis Cuba, USA, Argentina amaranthi C. cacti Echinopsis spp. India, Mexico C. chaubattia Malus sp. India Heterodera Bergenia ciliata Pakistan bergeniae *H. cajani Cajanus cajan, Glycine max, India, Egypt Phasealus spp., Pisum sativum, Sesamum indicum, Vigna sinensis, Phyllanthus maderaspatensis etc. H. cynodontis Cynodon dactylon Pakistan H. cyperi Cyperus esculentus, Cynodon USA, India, Mexico dactylon, H. delvii Eleusine coracana, Echinochloa India spp., , Zea mays H. elachista Upland rice Japan H. fici spp. China, former USSR, Bulgaria, Australia etc. H. gambiensis Sorghum, Pennisetum, Eleusine Gambia, India, Niger H. graminis Cynodon dactylon, Secale cereale, Australia, India, Trinidad, Setaria italica, Zea mays Fiji H. graminophila USA H. mothi Cyperus rotundus, Glycine max, India, USA, Iran, Iraq, Chrysanthemum, Hibiscus, cotton, Pakistan, Fiji sugar beet, sugar cane, onion, grapevine, almond, cherry, date palm, Cynodon dactylon H. oryzae Swamp rice, banana Ivory Coast, Thailand, USA, Senegal *H. oryzicola Upland rice, banana India H. pakistanensis Triticum aestivum Pakistan H. raskii Cyperus bulbosus India *H. sacchari Rice, sugar cane, Poaceae Congo, Ivory Coast, Nigeria, Senegal, Gambia, Burkina Faso, India, H. sinensis Imperata cylindrica China, Pakistan, Trinidad *H. sorghi Sorghum vulgare, Zea mays etc. India, Pakistan *H. zeae Zea mays, Poaceae India, Pakistan, Egypt, former USSR, USA, Thailand

• Most economically important species Heterodera 7 species above in terrns of non-specific esterase isozyme profiles and rnorphology (Nobbs, Ibrahirn and Rowe, 1992). This nernatode belongs to Mulvey's (1972) "Goettingiana" group rather than the "Schachtii" group, although in older literature it was taken tobe H. oryzae. Mulvey classified the cyst nernatodes into a series of five groups in which Group 1 included Punctodera and Globodera, Group 2 included Cactodera, Group 3 was the "Avenae" group, Group 4 was the "Schachtii" group, and Group 5 was the "Goettingiana" group. This systern has forrned the backhone of subsequent cyst nernatode groupings. At least 17 species of cyst nernatodes are found on the sub-continent of lndia (Sharrna and Swarup, 1983). Major crop losses occur on pulses and cereals, in particular pigeonpea and rnaize, on which darnage is caused by H. cajani and H. zeae, respectively. The host range of H. cajani includes Cajanus cajan, Phasealus spp., Sesamum indicum, Phyllanthus maderaspaten• sis and Pisum sativum, and has been reported frorn rnany Indian states (Koshy and Swarup, 1971a; Sharrna, Srnith and McDonald, 1992), Pak• istan and Egypt; it can also have up to nine generations a year (Koshy and Swarup, 1971b). is a very distinctive species which it would be difficult to rnisidentify because of the unique arrangernent of the four finger-like bullae that are always present in the cyst; Sharrna and Swarup (1984) described these bullae as "cross bullae". It is economically important and found throughout India (Sharrna and Swarup, 1983), and in Pakistan (Maqbool, 1980), Thailand (Chinnasri, Tangchitsarnkid and Toida, 1994) and the USA (Sardanelli, Krusberg and Golden, 1981). Het• erodera zeae was probably introduced into the USA (Baldwin and Mundo• Ocarnpo, 1991), where it is taken as a serious problern and quarantine rneasures are irnposed to prevent its spread to the com belt. The opti• rnum ternperature for hatch of H. zeae is 25 oc (Srivastava, 1980) and ternperatures of 10-15 oc reduce hatch to about 20% of rnaxirnurn (Sri• vastava and Sethi, 1985). Its prirnary host, as the narne irnplies, is rnaize and other hosts are Coix lachryma jobi, Eleusine coracana, Echinochloa colona, Hordeum vulgare, Panicum spp., , Setaria italica, Secale cereale, Sorghum vulgare, Triticum aestivum and Zea mexicana (Srivastava and Swarup, 1975; Sharrna and Swarup, 1984; Luc, 1986). Further record of Avena sativa as host has been reported but associations with Citrus spp., Prunus spp. and Lycopersicon esculentum arnong others (Shahina and Maqbool, 1995) seern rnore likely to be accidental than a reflection of true host status. seerns to consist of a nurnber of host races and pathotypes and is found in rnany countries around the world, spanning tropical, sub-tropical and ternperate zones. It seerns to have adapted to rnany environrnental situations. The "avenae cornplex" is referred to on the Indian sub-continent as the "Molya" cyst nernatode. There are popu• lations which seern to have surrnounted the problern of desiccation, 8 Distribution and economic importance unlike their temperate counterparts, such that populations in northem lndia can withstand dry conditions and temperatures of 30 oc. Some populations have adapted to temperate situations within tropical zones. Heterodera avenae survives well in South Australia on cereals (Brown, 1974) and also causes problems on cereals in China (D. Peng, personal communication). Much work on the virulence of H. avenae has been done in Sweden (Ireholm, 1994), Australia and India and there is recent infor• mation about the H. avenae complex from the former USSR, including information on H. filipjevi (Subbotin, Rumpenhorst and Sturhan, 1996). Heterodera avenae parasitizes and damages (Yadav and Verma, 1971; Gill and Swarup, 1971) as well as other cereals and possibly grasses. In the UK, andin many parts of northem Europe, H. avenae has become less important because natural control of this species seems to occur when cereals are grown continuously (Kerry, Crump and Mullen, 1982). Heterodera sorghi is found mainly in India and Pakistan parasitising sorghum, and its other hosts are Echinochloa colona, Eleusine coracana, Setaria italica, Paspalum scorbiculatum, Zea mays, Cyperus rotundus and Pennisetum typhaides (Sharma and Swarup, 1984). Sorghum has many uses but formspart of the human diet in India, Sudan and other parts of Africa. As is often the case with cyst nematodes, there is a closely related species with which H. sorghi can be confused morphologically, H. gam• biensis. Heterodera gambiensis has been reported as a parasite of sorghum in Gambia and of millet in Niger (Sharma, Waliyar and Ndunguru 1990) and is possibly better known for parasitising finger millet, as does H. delvii (Krishna Prasad et al., 1980). There is little information on H. gambiensis and its distribution may be limited to West Africa and India. Heterodera sinensis, a closely related species with H. gambiensis has been reported as a parasite of lelong grass in China (Chenand Zheng, 1994). Heterodera fici is a tropical species parasitising Ficus spp. When present in glasshouses it is capable of damage, particularly on young seedlings. It is one of the few cyst nematodes nottobe a parasite of Poaceae, Fabaceae, Chenopodiaceae or Cyperaceae. Its distribution is worldwide but it was first described from China (Kir'janova, 1954) and is also found in Bul• garia, North America, Australia, Brazil and several Mediterranean coun• tries. The species morphologically most similar to H. fici is H. humuli, a temperate species whose major host is hops, lupulus, although several workers (Memy, 1968; Mulvey, 1972) have found characters that differentiate the two. The so-called hop cyst nematode is known to have been present in the UK since at least the ninth century (Webley, 1974) but H. lupulus was not introduced to the UK until the 16th century. It is therefore assumed that H. humuli was living on a member of the Urtica• ceae or Moraceae before that time, but may only have been taken to the many other European countries in which it occurs on hop rootstocks when they were traded between countries. Heterodera 9 (b) Subtropical

Sorne of the countries of the Mediterranean and other areas that are dry and arid, such as the region araund Tashkent and parts of Japan, and which are not designated as tropical but can be extrernely hot with ternperatures of 30 oc to 40 oc, contain a nurnber of cyst nernatode species which tend tobe cornrnon to thern, such as H. ciceri, H. mediterranea, H. turcomanica and, often, H. latipons. Two of these four species are capable of serious econornic darnage, whereas H. mediterranea is known only frorn the Adriatic coast on the woody host Pistacia lentiscus, another exarnple of a cyst nernatode species found on trees, and H. turcomanica does not cause significant econornic darnage as it is recorded frorn Chenopodia• ceae in the desert. is reported as darnaging to chickpea in the north of Syria (Vovlas, Greco and Di Vito, 1986). Its preferred hosts are rnernbers of the Fabaceae and surveys rnade during 1979-80 suggest a 20% loss of yield due to this nernatode. The best known hosts are chickpea (Cicer arietinum), (Lens culinaris) and peas (Pisum spp.). Host tests have been done but, out of 14 botanical farnilies, rnost were very poor or non• hosts, with the notable exception of Dianthus cariophyllus. The distribu• tion of H. ciceri appears, as yet, tobe confined to Syria (Greco et al., 1986). (Franklin, 1969) is yet another species of cyst nerna• tode that parasitizes cereals including (Triticum aestivum), (Avena sativa), (Hordeum vulgare) and rye (Secale cereale), with the darnage to wheat the rnost irnportant. Heterodera latipons has a wide distribution: the type locality is Israel but it is also present in Italy, Bulgaria, Turkey, Syria, Libya and Iran. Sikora (1988) believes that the spread of H. latipons to North Africa and western Asia could have serious consequences. Heterodera turcomanica frorn Turkmeniya is close in rnorphological terrns to H. latipons (Sturhan and Wouts, 1995) and these two species were the only species in the now discredited genus Ephippiodera Wouts 1985, but the sirnilarity ends there. Heterodera latipons has only been reported frorn grarninaceous plants whilst H. turcomanica is restricted to hosts within the Chenopodiaceae. Also, re-examination of type prepara• tions of H. turcomanica frorn the Kara-Kurn desert revealed the presence of two other, new and undescribed, species, both of which would fit into the sarne rnorphological group as H. turcomanica and H. latipons, within the "avenae cornplex". Heterodera glycines was first described by Ichinohe (1952) on in Japan, although it was recognized rnuch earlier (Hori, 1915). It was discovered sirnultaneously in the USA where the hosts were thought to be weed species but, with the introduction of soybean, this becarne the preferred host. The distribution of H. glycines is wide, including Japan, 10 Distribution and economic importance China, the former USSR, Korea, Colombia, Brazil and Java (Riggs and Niblack, 1993). It is a very pathogenic species of cyst nematode which attacks plants mainly within the Fabaceae but is also capable of parasitis• ing non-leguminaus hosts such as Fensternon spp. and Verbascum thapsus in the Scrophulariaceae (Smart, 1964). Heterodera glycines is a member of the large "Schachtii" group of cyst nematodes and has many features in common with H. trifolii and H. lespedezae, particularly regarding host range. Morphological characters can be used to distiguish H. trifolii from H. glycines but H. lespedezae may also be present on soybean in the same geographic areas (Fagbenle, Edwards and Malek, 1986), so great care must be taken to make a correct diagnosis. Heterodera glycines con• sists of a number of races (Riggs and Schmitt, 1988) but the use of biochemical techniques to study variation within the species has revealed relationships that do not necessarily agree with the host preference classification (Baldwin and Mundo-Ocampo, 1991).

(c) Temperate was first observed by Schacht in 1859 (Franklin, 1951) and was the first cyst nematode to be described (Schmidt, 1871). Its distribution is worldwide and many species of cyst nematodes are grouped within the "Schachtii" group or Mulvey's Group 4 (Mulvey, 1972), which now contains at least 20 species. In the late 19th and early 20th centuries, most cyst nematode species were assigned to the species H. schachtii. However, H. schachtii reproduces only on Chenopodiaceae and Cruciferae, with few exceptions, but weeds can be almost as import• ant as crop hosts in maintaining populations of this species. Krall and Krall (1978) suggest that the epicentre for evolution of H. schachtii is within the Mediterranean area, also the centre of origin of many culti• vated plants. They express the view that weeds such as goosefoot were the primary hosts for H. schachtii, which then migrated to other species of Chenopodiaceae, such as beet, and the Cruciferae in the form of Brassica spp. Darnage by H. schachtii is of especial importance in the production of sugar beet in European countries and the former USSR. Heterodera schachtii is extremely difficult to separate, using morpholog• ical characters alone, from H. trifolii, H. glycines, H. galeopsidis, H. rosii and H. lespedezae. However, these species can be separated by biochemical methods, such as non-specific esterase gel electrophoresis, and by DNA analyses. Heterodera schachtii has been reported widely in Europe, the Middle East and the USA. It has also been reported from the Cape Verde Islands (Sturhan, 1993) on tomato, and host tests done in Germany on samples taken from St Vincent showed cysts parasitizing sugar beet and rape. It has not often been reported from South America but has been found in Heterodera 11 Mexico near the town of Chalco (Sosa-Moss, 1987) and it has been reported on beet and cabbage in a garden in Dakar, Senegal, and on beet in Gambia (Bridge and Manser, 1980). These latter cases are isolated but, nevertheless, the nematodes were established and, since these coun• tries have hot climates, this emphasizes the adaptability of this cyst nematode species. is not regarded as a major pest although it is a parasite of important Brassica spp. within the Cruciferae. It is unusual in that it can continue to develop on autumn-sown crops throughout the winter months (Stone and Rowe, 1976). Countries from which it has been reported include the UK, Bulgaria, Germany, Poland, Portugal and South Australia, so it has a wide distribution but a narrow hast range. is similar to H. cruciferae in having a fairly restricted hast range, parasitising mainly Daucus spp. within the Umbelliferae (Jones, 1950; Vallotton, 1980). The type locality is Chatteris in the UK but an earlier report of cysts on in Wiltshire, England (Triffitt, 1931) is thought tobe the first record of this species. There is usually only one generation per year but, if successive crops are grown, it can be very damaging, for instance in the Valado dos Frades area of Portugal (Reis, 1986) andin Germany (Sturhan, 1960). Other plant hosts, such as Torilis arvensis (Vallotton, 1980) and T. leptophylla (Mugniery, cited in Greco, 1986), within the Umbelliferae may act as a reservoir for cyst survival. Distribution of H. carotae is wide in Europe (Greco, 1986), including Cyprus (Philis, 1976), and there are also reports from the USA (Miller, 1986) and from cooler regions in tropical areas such as India (Swarup, Prasad and Raski, 1964). is a largely European cyst nematode, first found in Germany causing darnage to peas at the Agricultural Institute at Goettingen in 1890 (Franklin, 1951). The first record of H. goettingiana in the UK was on peas (Theobald, 1912), when it was identified as H. schachtii. Its hast range was first tested by Liebscher (1892), using plots at the Agricultural Institute at Goettingen. The many varieties of Pisum sativum he used showed this tobe a major hast; other hosts included Vicia Jaba, several other Vicia spp., Ervum leus, Lathyrus spp., Cicer arietinum, Lupinus luteus, L. cruickshankii, L. albus tenuis and Glycine hispida. Gaffart (1941) tested the hast range again with additional hosts on the same plots and found no cysts on , red or white clover, sugar beet, cereals or potatoes. Franklin (1951) reported that Phasealus vulgaris is notahastand Capus (1917) made the interesting observation that Fusarium vasinfectum was also present in most infections of H. goettingiana, causing footrot of peas. Since this time, of course, many more reports have been made of cyst nematodes and fungal diseases interacting to cause severe darnage in crops. 12 Distribution and economic importance was also described in the early years of plant nema• tology and appears tobe closely related to H. glycines, H. schachtii and H. galeopsidis. There are a nurober of races within H. trifolii that are morpho• logically identical but separable by their ability to multiply on different hosts (Mulvey and Anderson, 1974). The host range of H. trifolii extends to at least 110 species and includes clover, Rumex spp., Stellaria media, Galeopsidis speciosa and Isatis tinctoria, with Brassica alba and Beta vulgaris recorded as minor hosts. At one time, it was thought that the H. trifolii 'complex', tagether with H. rosii and H. galeopsidis, could be differentiated from H. schachtii by the yellow phase prior to the tanning of the female and that this was a good diagnostic feature as H. schachtii usually has white females. However, a race of H. schachtii has been reported to have a similar yellow phase (Stone, 1983), so leaving host range as the only definitive diagnosis until, for instance, biochemical systems of diagnosis are worked out. Heterodera trifolii is a very cosmopolitan species, being not only distrib• uted throughout Europe, the former USSR, the USA, IsraelandIndia but also able to live in places with very high temperatures. It has also been reported from south-east Queensland, Australia, in association with fungi causing the death of Trifolium repens (Irwin and Jones, 1977).

1.2.2 Globodera This genus can be divided into three separate groups: (i) the species ( and G. rostochiensis) that originate from Andean regions of South America (Evans, Franeo and de Scurrah, 1975; Kralland Krall, 1978; Baldwin and Mundo-Ocampo, 1991) and parasitize potato and other closely related plant species within the Solanaceae, (ii) the species that form the G. tabacum group and also parasitize members of the Solanaceae, notably tobacco, and (iii) a small group of three species known only from members of the Asteraceae, which are markedly dif• ferent from other Globodera species in terms of cyst morphology and which are reported only from the former USSR, China, Japan, Germany and the UK. The species G. zealandica, however, fails to fit into this grouping. The genus Globodera was so-named first by Skarbilovich (1959) and this namewas resurrected by Behrens (1975). The cyst nematodes from pota• toes were originally described as Heterodera rostochiensis by Wollenweher (1923); this species contained the two species, G. pallida and G. rostochien• sis, with which we are familiar today. The first record of cyst nematodes on potatoes was by Kühn (1881) but, at this time, all cyst nematodes were still referred to as Heterodera schachtii. Zimmermann (1914) was the first to associate darnage to potatoes specifically with cyst nematodes. There was much confusion over the host and the name of the cyst nematode species Globodera 13 and, after the erection of H. rostochiensis by Wollenweber in 1923, potato cyst nematodes were named H. schachtii forma solani by Zimmermann (1927) and then re-named H. schachtii ssp. rostochiensis (Woll.) by Kemner (1929). By this time, potato cyst nematodes were well known from Scot• land (Massee, 1913) and the north of England (Strachan and Taylor, 1926) but Wollenweber's description of a separate species attacking potatoes was not accepted until Franklin (1940) described morphological differ• ences that separated it from other species of cyst nematodes and restored Wollenweber's specific name. Although potatoes were probably brought to Europe from South America in the 16th century by the Spanish, it seems likely that potato cyst nematodes were not brought to Europe until the middle of the 19th century (Evans and Trudgill, 1978), when new varieties of potato were introduced as breeding material after the Irish potato famines of the 1840s. Potato cyst nematodes are indigenous in Peru and other adjoining Andean countdes and were almost certainly common on potatoes in pre• Incan times, being still present on ancient, no longer cultivated terraces on the host Solanum acaule (Jatala and Garzon, 1987). Europe acted as a secondary distribution centre as potato cyst nematodes were carried to other countries around the world on seed potatoes. On a world basis, potatoes are one of the most important food crops, generally grown in temperate areas but also in tropical latitudes where altitude moderates the temperature. Thus, potatoes are grown under temperature regimes to which potato cyst nematodes are adapted. However, of the two species, G. pallida seems to be adapted to somewhat lower temperatures than G. rostochiensis as hatching of G. pallida begins at lower temperatures (Mugniery, 1978). Potato cyst nematodes and the G. tabacum complex all have evolution• ary ties with the plant family Solanaceae. For potato cyst nematodes, Solanum tuberosum, S. melongena and Lycopersicon esculentum are major crop hosts, and many other tuberous Solanum spp. are hosts (Stone, 1972) whilst weed hosts include S. nigrum, S. dulcamara, S. capsicastrum and Atropa belladonna. has also been recorded as a pathogen of tobacco in Venezuela (Meredith, 1976), andin in vitro experi• ments tobacco has also been recorded as a host for G. pallida (Parrott and Miller, 1977). The G. tabacum complex is found mainly in the USA and China and is also reported from the former USSR.It is not found on S. tuberosum but is a pest of tobacco, which has been grown as a crop for many years in South America, Central America, Cuba and the southem USA (Akehurst, 1981). also parasitizes solanaceous weeds where it occurs but is only a major tobacco pest in certain areas. lt is important in the USA, and in Colombia, France, Greece, ltaly, Korea, Morocco, Thailand and Yugoslavia (Shepherd and Barker, 1990). 14 Distribution and economic importance At one time, there were three individual species, G. solanacearum, G. tabacum and G. virginiae within what is now the G. tabacum complex (Stone, 1983). Also included is a species from Mexico which is synon• ymaus with G. virginiae. The morphology of this complex is very similar to that of the potato cyst nematodes, although the annulation of the area between the anus and the fenestra tends to be wavy in the G. tabacum complex and regular in potato cyst nematodes and there are subtle differences in female colour and stylet knob shapes of second stage juveniles. Biochemical analyses have revealed differences between Glo• bodera species, including an isolate from Bolivia once thought to be G. rostochiensis with virulence to certain solanaceous resistance genes but morphologically closer to G. pallida. Globodera species from the Asteraceae, G. achilleae and G. artemisiae have been described from Europe and the former USSR respectively; G. achil• leae has been found in the UK and Serbia. Globodera millefolii, however, is regarded by Krall (1977) and Stone (1977) as a species inquirenda. The species G. hypolysi, collected from Artemisia princeps in potato fields, was described by Ogawa, Ohshima and lchinohe (1983), but this species seems very close to G. artemisiae and may not be valid.

1.2.3 Punctodera Species of the genus Punctodera originally belonged to the genus Hetero• dera but Mulvey and Stone (1976) created the new genus, which contains only three species: P. punctata, P. matadorensis and P. chalcoensis. The latter is the most important species, causing important losses to maize in Mexico. Punctodera punctata was described from wheat in Saskatchewan in Canada by Thome (1928) as Heterodera punctata and is indigenous to the UK where it has been found on Agrostis spp. of grass; it has also been reported on wheat in other parts of Canada and there is a record of young cysts and females parasitizing roots of maize from Serbia (Grujicic, 1969). Neither P. punctata nor P. matadorensis seem to cause much crop darnage or yield loss but P. punctata is of significance when it is found in temper• ate areas where solanaceous crops are grown when it could be mistaken for Globodera spp. and cause inappropriate control decisions to be made. Although cysts of P. punctata and P. matadorensis are usually ovoid and smaller than those of Globodera spp., those of P. chalcoensis are darker in colour, larger and round, and therefore more difficult to diagnose when found in Mexican valleys close to potato production areas. The most reliable procedure is to examine the anal region of individual cysts when two distinct fenestrae will be seen in cysts of Punctodera, one containing the anus, the other the vulval slit. The hosts of P. chalcoensis are Zea mays and teosinte, thought to be the precursor of maize and found mainly as weeds in maize fields. Darnage is Cactodera 15 most severe if the rains come as seedlings are just growing as the rain seems to stimulate hatch and subsequent root invasion. The resulting root darnage encourages infection by secondary pathogens and infected plants are chlorotic and stunted, with yield losses of up to almost 100% (Baldwin and Mundo-Ocampo, 1991). Punctodera matadorensis has only been reported from its type locality in Canada on weed grasses. It can be separated from P. punctata in having larger cysts containing large bullae and by not parasitizing wheat. Other work (Rumpenhorst, 1985) has shown biochemical variation within P. punctata but little work has been done on this genus, largely because it is of little economic importance and damaging populations can either be treated with nematicide or their effects counteracted with supplementary nutrients (Sosa Moss and Gonzalez, 1973).

1.2.4 Cactodera The genus Cactodera was erected by Krall and Krall (1978) with type species C. cacti synonymaus with Heterodera cacti Filipjev and Schuur• mans Stekhoven, 1941. This species was first noted on Phyllocactus akker• manni and Cereus speciosa by Adam (1932), who passed the cysts on to Goffart, who believed that they belonged to a strain of H. schachtii adapted to cacti (Goffart, 1936), despite the spherical shape of the cysts, their yellow phase during maturation, the low vulval cone and the absence of an egg sac, as detailed by Franklin (1951). There are nine species of Cactodera which parasitize hosts within the Cactaceae, Chenopodiaceae and Amaranthaceae and two other species, C. betulae which parasitizes birch oralder trees (Hirschmann and Riggs, 1969; Golden and Raski, 1977), and C. chaubattia recorded from soil in association with apple trees (Gupta and Edward, 1973). Members of this genus are believed to have evolved in or close to Mexico (Kir'janova and Krall, 1969, 1971). is found on native plants throughout Argentina, Brazil, Colombia, Mexico and parts of the USA. Cactodera amaranthi is also common in this part of the world, having been reported from Amaranthus viridis in Cuba (Stoyanov, 1972) and spinach and com• mon weeds in central Mexico (Sosa Moss, 1987). The genus is also well represented in temperate regions in the form of C. estonica and C. cacti, which have been found in many European countries in glasshouses on ornamental plants. No studies on the effects of Cactodera species on their hosts have yet been made, largely because they do not seem to be important economic pests. The only possible situation where they may be a problern is in Mexico where Opuntia is grown as a commercial crop and the cyst nematodes might cause direct crop darnage or encourage infection by secondary pathogens (Baldwin and Mundo-Ocampo, 1991). 16 Distribution and economic importance 1.2.5 Non-cyst-forming and ancestral members of the Heteroderinae

Lesser known, non-cyst-forming species of the Heteroderinae (Table 1.3) deserve mention as awareness of them has increased over the last decade, because of their phylogenetic importance and the possibility that some of them cause important crop lasses, for example Meloidodera floridensis (Hutchinson and Reed, 1959). Same of the genera are represented by just one species each viz. Ekphymatodera, Hylonema, Camelodera etc. Ofthis group, Verutus and, to a lesser extent, Meloidodera are regarded as the ancestral members because of the ancestral characters they display, such as the situation of the vulva at mid-body and annulation of the entire body surface (Luc, Maggenti and Fortuner, 1988). Three species of Verutus are now recognized and some nine species of Meloidodera. Fernales of Meloidodera are usually encapsulated in a proteelive nodule made up of roots, fungi and cuticular debris (1. Cid del Prado, personal communication). Species of the genus Meloidodera have a variety of hosts: M. mexicana and M. charis both parasitize corn and M. floridensis has been shown to parasitize roots of Pinus rigida and P. echinata in New Jersey, USA (Hutchinson and Reed, 1959). In 35 Southern Pine nurseries, M. floridensis was found to parasitize Pinus clausa, P. nigra, P. palustris and P. taeda, with P. clausa severely damaged at one site (Hopper, 1958). Pinus elliottii was shown to suffer darnage from M. floridensis in pot tests (Ruehle and Sasser, 1962). Cryphodera could also be considered as ancestral on the basis of its cuticle annulations and lack of a posterior protuberance (Baldwin and Mundo-Ocampo, 1991). Four species of Cryphodera are parasites of trees in New Zealand and Australia. Verutus has a wider distribution, with the type species, V. volvingentis, described from Button Weed in Florida (Esser, 1981) and another species described from mainly graminaceous hosts in California. Bilobodera flexa has been described from Andhra Pradesh, India on the hast Allmania nodiflora and other members of the Amaranthaceae (Sharma and Siddiqi, 1992). This species also has ances• tral characters. Afenestrata and Dolichodera do form cysts, with just one species of Dolichodera, reported from Quebec (Mulvey and Ebsary, 1980), from an unknown hast as the cysts were found in river sediment. There are five species of Afenestrata: A. africana, A. sacchari, A. koreana, A. axonopi and A. orientalis, from Africa, Korea, Brazil, the former USSR and India parasitizing Poaceae. Brevicephalodera bamboosi is also cyst-forming and is found on Bambusa sp. roots in the district of Jorhat, Assam, India. The remaining non-cyst-forming members of the Heteroderinae com• prise the Sarisoderines, Sarisodera, Rhizonema, Bellodera, Hylonema and Ekphymatodera. Four of these genera are found only in the western USA, Economic importance 17 the exception being Hylonema from the Ivory Coast. The host preference of Ekphymatodera for rushes is not in keeping with the rest of this group, whose main hosts are trees and woody shrubs. The Ataloderines consist of Atalodera, Thecavermiculatus and Camelodera, and are grouped together because of morphological similarities and because they form syncytial feeding sites (unlike most other non-cyst forming Heteroderidae) which lack wall ingrowths (Mundo-Ocampo and Baldwin, 1983). The number of described species in these minor groups will grow in time, because they tend to inhabit undisturbed habitats and are small and easily missed during sample processing. As more sites are more carefully sampled more species will be recognised.

1.3 ECONOMIC IMPORTANCE An analysis of the host range and actual amounts of darnage caused, taken in conjunction with knowledge of the bionomics of members of the various genera, allows an assessment of the economic importance of each group of species within the Heteroderinae. Heterodera is by far the largest genus of cyst-forming species, with Poaceae one of the commonest plant families to act as hosts (of some 25 species). Host potential actually cuts across Mulvey's grouping of the "Avenae", "Goettingiana" and "Schachtii" groups on a morphological basis. All members of the Avenae group parasitize Poaceae, with the exception of H. turcomanica which parasitizes members of the Chenopod• iaceae. Some of the species within the A venae group are very damaging, viz. the H. avenae complex, H. filipjevi and H. latipons, whilst species such as H. mani (which the authors consider a valid species), H. arenaria and H. iri seem to persist in equilibrium with their hosts, causing no agricultural problems. The Goettingiana group, as defined by Mulvey (1972), contains at least eight species which parasitize graminaceous hosts, although the main hosts of this group are within the Fabaceae and Cruciferae. The two most damaging species in this group to parasitize Poaceae are probably H. elachista on rice and H. pakistanensis on wheat. Within the Schachtii group, the species with graminaceous hosts para• sitize rice, sugar cane and maize. This group probably contains the most species regarded as devastating and it is almost easier to list the species which are least damaging to plants, viz. H. leucilyma, H. limonii and H. rosii. Virtually all other species within the Schachtii group are of signific• ant economic importance. The three species of Punctodera are all parasites of Poaceae and only one, P. chalcoensis, seems tobe of economic significance and that only on maize in Mexico. The darnage it causes is of particular significance because maize is a staple crop in Mexico. 18 Distribution and economic importance Cactodera is currently of no economic significance but C. cacti might become so where cacti are grown as food crops and in glasshouses where ornamentals are housed or grown commercially. Other species of Cacto• dera are widely distributed but do not cause damage, although some stunting and discolouration have been reported (Stelter and Kuhn, 1973). In contrast, Globodera species can be extremely damaging. The most important are the two species of potato cyst nematodes, which cause severe darnage to potato crops ranging from barely noticeable up to total crop loss. Overall lasses to these species in the UK have been estimated at about 9% of crop production (Evans and Stone, 1977) and similar lasses must occur in many of the at least 58 countries in which potato cyst nematodes are known to occur (EPPO, 1992). The species of cyst nematodes of major economic importance in temperate regions are listed along with the main crops affected (Table 1.5). The total economic lasses caused by cyst nematodes are virtually

Table 1.5 Temperate cyst-nematodes of major economic importance

Genus Species Crops affected Globodera pallida Potatoes, Tomatoes, eggplant rostochiensis } Heterodera avenae Wheat, Barley, , grasses ciceri Chickpea carotae Carrots cruciferae Brussels sprouts, Broccoli, Cabbage, Cauliflower, Kale, Kohlrabi, Peas, Rape, Rutabaga, Turnip, various ornamentals glycines Adzuki bean, Broad bean, French bean, Hyacinth bean, Kidney bean, Moth bean, Mung bean, Navy bean, Rice bean, Snap bean, Soybean, Blackgram, Cowpea, Sesame, White lupin, Yellow lupin. goettingiana Broad bean, Chickpea, Lentil, Peas, White lupin, Yellow lupin. schachtii Adzuki bean, Beet, Broccoli, Brussels sprouts, Cabbage, Cauliflower, , Chickpea, Chicory, Chinese cabbage, Cowpea, Dill, Kale, Kohlrabi, Lentil, Peas, Radish, Rape, Rhubarb, Rutabaga, Spinach, Tomato, Turnip, Yellow lupin, various ornamentals. trifolii Beet, Carnations, Chickpea, Cucumber, Gherkins, Peas, Pumpkin, Red clover, Rhubarb, Spinach, Squash, Tomato, White clover, White lupin, Zucchini. Quarantine 19 impossible to evaluate, especially as many factors such as soil type, other pathogens and climate influence the losses caused in the field. Estimates of losses under controlled conditions can only suggest how much darnage might be caused in practice and field estimations are often inaccurate. A farmer has to consider carefully the effects of nematodes on his crops as the potential benefit of any control measure must exceed the cost of that measure. Cyst nematodes are a special case in that they are usually capable of persisting for many years in soil and a farmer must consider the long-term implications of his actions as well as the immediate effects on any crop. In extreme circumstances, no suitable control measures may be available and the end resort may be re-location to a cyst-nematode-free site. To the consumer, loss of yield to nematode attack will mean higher prices, scarcity of the commodity and perhaps a decline in quality.

1.4 QUARANTINE Quarantine, with reference to plant parasitic nematodes, is best defined as those restrictions that are placed upon the production and movement of plants and plant products in an attempt to prevent the introduction or limit the spread of alien nematode pests or to limit the spread of an established nematodepest (see Cotten and Van Riel, 1993).1ts imposition is necessarily on a large scale and therefore expensive, with no immediate economic retum. However, the long-term benefits are potentially very large. For instance, expenditure of many millions of dollars on the USDA Golden Nematode project seems to have limited its spread within the USA to relatively few locations so far (Brodie, Evans and Franco, 1993) and to have completely prevented the introduction of the more danger• ous of the two species, G. pallida. Proper implementation of quarantine regulations requires accurate identification of pest species, for instance in attempting to detect small numbers of G. pallida in mixtures with G. rostochiensis. This has been aided by modern methods of diagnosis such as isoelectric focusing (Fleming and Marks, 1983), which allows up to 100 cysts to be checked easily and quickly, in contrast to identification by light microscopy which would be tedious, require considerable experience and expertise, and permit no more than 5 to 10 cysts tobe checked per sample. This has obvious implications for the chances of detecting a noxious species occurring at low frequency in a species mixture. In a similar manner, it is possible mistakenly to identify a benign species of nematode as a pest species and this is where, for instance, the Globodera species parasitic on Asteraceae may assume significant importance even though they cause no economic darnage themselves (e.g. G. hypolysi found in potato fields in Japan (Ogawa, Ohshima and Ichinohe, 1983)). If their cysts are found 20 Distribution and economic importance contaminating a potato seed shipment supposedly free of potato cyst nematodes and are mistakenly identified as those of potato cyst nema• todes, then the shipment may be unjustifiably rejected, at considerable cost to the producers. Various organizations around the world help in the implementation of phytosanitary regulations. Certain physical barriers or specific environ• mental requirements help to confine some pest species to their places of origin but modern trade is largely responsible for the unwanted move• ment of pest species of nematodes. The European Plant Protection Organ• isation (EPPO) oversees the prevention of importation of noxious pests and diseases and produces an Al list of pathogens not present within EPPO countries whose entry must be vigilantly prevented, and an A2 list of pathogens already present in some EPPO countries whose further spread must be prevented. The USA and Asian and Pacific countries have their own plant protection organizations with the same aims as EPPO. Some countries even require allplant imports tobe bare-rooted and this is very relevant to cyst nematodes as soil is usually the vehicle by which new infestations are started. Any means by which soil may be transported can transfer cysts to previously uninfested land, and this includes the transport of soil on farm equipment and even farm workers' feet as well as the use of planting stock grown in contaminated soil. Thus, where particular nematodes are identified as risks, legislative controls can slow their rate of spread and perhaps allow time for the development of alternative methods of control such as appropriate resist• ant cultivars.

1.5 CONCLUDING REMARKS In the early days of plant nematology, cyst-forming and related genera of the Heteroderinae were considered to be pathogens of temperate regions of the world with few, if any, real problems arising in tropical and sub• tropical regions. Some of the early observations of cyst nematodes from non-temperate regions were thought to be misidentifications, such as a report of cyst nematodes in the Hawaiian islands (Muir and Henderson, 1926, cited in Luc, 1986); the record was queried by Goodey (1956) who attributeditto a misidentification and suggested that it was a Meloidogyne sp. To some extent, this is understandable as cyst and root-knot nema• todes were at one time grouped together as Heterodera marioni (Cornu, 1879) following their discovery by Berkeley in 1855 (Franklin, 1951). Today, we are aware of many more species of Heterodera and genera within the Heteroderinae but there are still some problems of classifica• tion and workers with substantial experience of all the groups and species within them are already rare and becoming rarer. Set against this is the increasing use of highly technical methods in but, Concluding remarks 21 despite the argument that the results from such methods are more object• ive, as this technology becomes more complex the challenge to interpret the findings becomes increasingly complicated. In taking advantage of new technology, we must ensure that records and reports from the pre• computer era are not lost. Some of these records are very important and are as valid now as they werein the past. However, personal knowledge of the subject must also be updated in order that changing criteria can be applied and correct interpretations made. It is likely that more and more "species complexes" will be described and, with the advent of eheaper travel, electronic mail and generally better methods of communication, even workers in the more remote regions of the world will become easy to communicate with and information exchange may well lead to the synonymization of some of the current species. Correct training is of great importance when it is planned to survey a previously unexplored area, even down to how and where samples should be taken and which extraction method to use. Poor facilities often mean that the chosen extraction method is a variant of the Baer• mann funnel technique. This will not extract cysts and, since many cyst nematode species do not hatch readily in water, the short time for which the cysts are in contact with water may not be sufficient for juveniles to emerge and their presence may go unnoticed. As nematologists lookfurther and harder for cyst nematode species, so the distribution of this group seems to extend; for instance, H. zeae was recently found on maize in Thailand (Chinnasri, Tangchitsamkid and Toida, 1994). However, in an exhaustive survey of agricultural crops in the Central and South Pacific during 1976 and 1977, only 1% of species found were heteroderid (Orton-Williams, 1980); cysts were not recovered with the exception of two species from Fiji, Heterodera graminis and H. mothi (Kirby et al., 1978). Without the mature cyst characteristics, it is impossible to decide which species is present and its potential agricul• tural significance. A good example of this is when Heterodera-like juve• niles were found in samples but only after extensive searching were they found to come from a new non-cyst-forming species Hylonema (Luc, Taylor and Cadet, 1978). There are many other reports of Heterodera-like juveniles coming from unknown sources (Sharma and Swarup, 1983). The main host families given in Table 1.1 are generally the most important. However, the economic importance of a nematode species cannot be predicted by looking at one member of a botanical family (usually the type host). Some examples of cyst nematodes where host range testing has revealed much more important hosts than the type host are: Heterodera graminophila, described from Bermuda grass (Echinochloa colona) but shown to parasitize Oryza sativa and Sorghum halapense (Birchfield, 1973); H. graminis, found on a variety of grasses in New South Wales (Stynes, 1971) but shown to reproduce on maize, Table 1.6 The geographical distribution based on type locality of species of heteroderid nernatodes, within each genus, including both cyst- and non-cyst-forrning species

Europe Asia Africa Former USSR Mediterranean Australasia S. America N. America Globodera 1 1 1 1 3 1 Punctodera 3 Heterodera 19 15 3 19 4 3 4 Cactodera 1 (Estonia) 1 2 2 5 Dolichodera 1 Other Heteroderinae Cyst-forrning Afenestrata 2 1 1 Non-cyst-forrning Sarisodera 1 Atalodera 2 4 Cryphodera 1 4 Verutus 1* 2 Camelodera 1 Brevicephalodera 1 Bilobodera 2 Meloidodera 3(3) 1 2 3 Bellodera 1 Ekphymatodera 1 Thecavermiculatus 1 3 Hylonema 1 Rhizonema 1

* undescribed (inquirenda) References 23 Italian millet, Russian rye (Sharma and Swarup, 1984), oats and wheat; H. cynodontis, from Cynodon dactylon (Shahina and Maqbool, 1995) has been found in association with wheat, barley, maize, sorghum and soybean in Karachi (Shahina and Maqbool, 1995); H. mothi, described from Cyperus rotundus but reported on soybean, cotton, sugar beet, sugar cane, grape• vine and date palm in northern Iraq (Stephan, Alwan and Antoone, 1985), and onions, barley, wheat, eggplant, and other crops in Pakistan (Shahina and Maqbool, 1995). This underlines the ability of cyst nematodes, espe• cially Heterodera spp., to adapt to a variety of hosts although, as already mentioned, misidentification can sometimes lead to unusual records. However, some species of cyst nematodes seem to have very narrow host ranges. For example, H. limonii is known only from sea lavender and is the only species of cyst nematode known to parasitize a member of the plant family Plumbaginaceae, and similarly H. urticae only parasitizes Urticaceae, although more cyst nematode species may eventually be found on these hosts, of course. Stelter (1984) produced a list of cyst nematode species and compared that list with one he produced 13 years earlier. An updated summary of that information is presented in Table 1.6, which gives an indication of the current overall distribution of the genera which make up the Hetero• derinae. Wherever cyst nematodes are found, it is a generalization that the number of generations per year increases as the temperature increases, providing the upper threshold temperature for nematode development is not exceeded. Most temperate species of cyst nematodes will produce one or two generations when a host crop is grown. In the tropics, multiple generations are usual, with H. cajani reported to produce up to nine generations per year (Koshy and Swarup, 1971b) and H. oryzicola up to 11 Gayaprakash and Rao, 1983). Some "universal" species, such as H. avenae, appear tobe very adaptable to different environments with some races much better able to tolerate dry conditions than others. However, most species seem to have distinct preferences in terms of environmental conditions and this means that cyst nematodes have suc• cessfully colonised many different environments, with the consequence that many and varied control strategies are required to deal with them.

1.6 REFERENCES Adam, W. (1932) Note sur Heterodera schachtii Schm. parasite des . Bulletin du Musie d'Histoire naturelle de Belgique, 8, 1-10. Akehurst, B. C. (1981) Tobacco, 2nd edition, Longman, London and New York. Babatola, J. 0. (1983) Rice cultivars and Heterodera oryzae. Nematologia Mediterra• nea, 11, 103-5. Baldwin, J. G. and Bell, A. H. (1985) Cactodera eremica n.sp., Afenestrata africana (Luc et al., 1973) n.gen., n.comb. and an amended diagnosis of Sarisodera Wouts and Sher, 1971 (Heteroderidae). Journal of Nematology, 17, 187-201. 24 Distribution and economic importance Baldwin, J. G., Bernard, E. C. and Mundo-Ocampo, M. (1989) Four new species of Heteroderidae including Ekphymatodera n.gen. from California. Journal of Nema• tology 21, 48-68. Baldwin, J. G. and Mundo-Ocampo, M. (1991) Heteroderinae cyst and non-cyst forming nematodes, in Manual of Agricultural Nematology (ed W.R. Nickle), M. Decker Inc., New York, pp. 275-362. Baldwin, J. G. and Schouest, L. (1990) Comparative detailed morphology of Heteroderinae Filipjev and Schuurmans Stekhoven, 1941, sensu Luc et al., 1988 for the phylogenetic systematics and revised classification. Systematic Parasitology, 15, 81-106. Behrens, E. (1975) Globodera Skarbilovich, 1959. Eine selbständige Gattung in der Unterfamilie Heteroderinae Skarbilovich, 1947 (Nematoda: Heteroderidae). Vortragstagung zu Aktuellen Problemen der Phytonematologie, 12-26. Rostock, May 29, 1975. Birchfield, W. (1973) Pathogenesis and host parasitic relations of the cyst nema• tode Heterodera graminophila on grasses. Phytopathology, 63, 38--40. Bridge, J. and Manser, P.D. (1980) The beet cyst nematode in tropical Africa. Plant Disease, 64, 1036. Brodie, B. B., Evans, K. and Franco, J. (1993) Nematode parasites of potatoes, in Plant Parasitic Nematodes in Temperate Agriculture, (eds K. Evans, D. L. Trudgill and J. M. Webster), CAB International, Wallingford, pp. 87-132. Brown, R. H. (1974) Further sturlies on the Victorian biotype of the cereal cyst nematode (Heterodera avenae). Australian Journal of Experimental Agriculture and Husbandry, 14, 394-98. Capus, J. (1917) Sur un deperissement des cultures de pois en Girondeduala double action de l'Heterodera schachtii et du Fusarium vasinfectum. Bulletin Societe Zoologique Agriculture. Bordeaux, 16, 70-73. Charles, J. S. and Venkitesan, T. S. (1984) New hosts of Heterodera oryzicola Rao and Jayaprakash 1978 in Kerala, India. Indian Journal ofNematology, 14, 181-82. Chen, P. S. and Zheng, J. W. (1994) Preliminary report on a new species - Heterodera sinensis sp. Nov. from China. Scientia Agricultura Sinica, 27, 88. Chinnasri, B., Tangchitsamkid, N. and Toida, Y. (1994) Heterodera zeae on maize in Thailand. Japanese Journal of Nematology, 24, 35-38. Chitwood, B. G., Hannon, C. I. and Esser, R. P. (1956) A new nematode genus, Meloidodera, linking the genera Heterodera and Meloidogyne. Phytopathology, 46, 264-{)6. 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