Aphelenchoides ritzemabosi
(Chrysanthemum foliar eelworm)

A. ritzemabosi is one of the species which are presently targeted in regulatory programmes worldwide (O'Bannon and Esser, 1987).

The results of more than 8 years of voluntary certification schemes for strawberry stocks in Italy indicate that A. ritzemabosi, A. fragariae, D. dipsaci and Meloidogyne spp. can be successfully controlled by means of plant certification schemes (Tacconi and Lamberti, 1994).

A. ritzemabosi is a major and widespread pest of chrysanthemum in Europe, North America, South Africa, New Zealand and Australia, and has been reported on this host from several other countries including Brazil (Curi and Pitta, 1971), Mexico (Cid del Prado and Sosa-Moss, 1978; Sandoval Hernandez and Teliz Ortiz, 1990), Fiji (Swaine, 1971), Mauritius (Orian, 1957) and others (see Geographic Distribution).

Chrysanthemum is the major host in Europe (Juhl, 1978; Farkas et al., 1985); chrysanthemum, narcissus and pseudonarcissus are the main hosts in Italy (Vovlas and Lamberti, 1973); chrysanthemum and dahlia are major hosts in Poland (Szczygiel and Hasior, 1972). This species is also important on chrysanthemum in Japan (Kobayashi et al., 1971) and areas of China (Li and Zhang, 1992).

A. ritzemabosi and A. fragariae occur on and cause damage to strawberries in Denmark (Lindhardt, 1967; Andersson, 1969), England (MAFF, 1970), Switzerland (Klingler, 1969; Staubli et al., 1989); Germany (Hirling, 1970, 1971; Blank, 1985), Italy (Tacconi, 1972) and Poland (Szczygiel, 1967, 1970). A. ritzemabosi and A. fragariae are widespread in strawberry fields in Mexico (Szczygiel and Cid del Prado-Vera, 1981; Sandoval Hernandez and Teliz Ortiz, 1990). A. ritzemabosi occurs in strawberry plantations in southern Ukraine, USSR (Lebedeva et al., 1972), in the Crimea (Lebedeva and Metlitskii, 1972) and Bulgaria (Stoyanov, 1975).

The nematode has been reported on blackcurrant, dahlia, lavender, Callistephus, and many other cultivated plants in England (Franklin, 1959). In the UK, recorded hosts are: Allium flavum, Allium sikkimense, Buddleia spp., Ceratostigma willmottianum and Lewisia (Southey, 1974); Bergenia (Roberts, 1981); and Viburnum x bodnantense, cv. Aberconway Dawn (Southey and Roberts, 1977). It has also been recorded on lucerne and dry bean (Phaseolus vulgaris) in Western Europe (Franc et al., 1996); on dahlia in Italy (Lamberti et al., 1987) and on basil (Ocimum basilicum) in north-west Italy (Lamberti and Garibaldi, 1977); on Limonium sinuatum in Chile (Bohm and Aruta, 1985); and on china aster (Callistephus chinensis) in Germany (Burckhardt, 1972). Also recorded as hosts are: tobacco (Nicotiana tabacum) (Grujicic, 1972; Weischer, 1975; Sikora and Dehne, 1979); Rumex spp. and Echium in Madeira, Rumex spp. and Geranium in the Canary Islands (Sturhan, 1973); the fungus Rhynchosporium verticillatum, Ipomoea purpurea [Pharbitis purpurea] and Aster sp. in Simla, India (Ahmad, 1971); Zinnia elegans, Salvia splendens, chrysanthemum and dahlia in hilly regions of northern India (Gill, 1981; Khan et al., 1987).

A. ritzemabosi was recorded on redcurrant and boysenberry in New Zealand (Dale, 1971); for the first time on the following plants: Aster dumosus, Campanula pyramidalis, cultivated Dahlia, Helleborus niger, Hibiscus rosa-sinensis, Marattia salicifolia, Passiflora edulis, Ranunculus sardous, Rheum rhaponticum and Zinnia elegans by Boesewinkel (1977); on Aquilegia vulgaris by Boesewinkel (1980); on Lotus corniculatus, Lycopersicon esculentum, Phytolacca octandra, Senecio petasitis and Tristania conferta by Boesewinkel (1982). A. ritzemabosi was found on lucerne and dry bean (Phaseolus vulgaris) in Wyoming and other western states of the USA (Franc et al., 1996); on gloxinias (Sinningia speciosa) in Florida (Lehman, 1991) and on pinto bean (Phaseolus vulgaris, var. Othello) in Wyoming, USA (Franc et al., 1993). The nematode has also been recorded in the USA on African violet (Saintpaulia ionantha) (Strider, 1979); Verbena (Christie, 1959); gooseberry, lupin, Mimulus guttatus, Saintpaulia, watermelon and Peperomia (Allen, 1952). Christie (1959) stated that at least 25-30 different plant species are hosts in the USA, including Aster, Calceolaria, Dahlia, Delphinium, Phlox, tobacco, Verbena and Zinnia. It is also widespread on Zinnia in South Africa (Wager, 1972).

Juhl (1978) gives a list of 249 plant species in Denmark which are hosts for A. ritzemabosi. Two ferns, Asplenium nidus and Struthiopteris orientalis, and one fungus, Rhynchosporium verticillatum, are also hosts for the nematode (Juhl, 1978). Wallace (1961) reported 190 plant species as hosts, and Sturhan (1962) recorded it on 31 new hosts, mostly in Compositae, in Germany.

A. ritzemabosi is an obligate plant parasite, inhabiting leaves, buds, growing points and outer layers of stem; in soil it does not complete its life cycle or survive the winter. It feeds endoparasitically on mesophyll cells of leaves, and ectoparasitically on buds and growing points (Southey, 1952; Siddiqi, 1974). The nematodes move in the water film over plants, not within the stem tissue, to reach the leaves and buds. Rain splashes and leaf contacts contribute to re-infestation and spread (Wallace, 1959). The leaves are invaded through the stomata. The nematodes feed on the parenchymatous tissue of the mesophyll and destroy the cells, resulting in leaf spots or blotches, easily seen on the under surface. The nematodes leave brown tissue through the stomata and migrate in the water film on the surface to infect terminal flower buds which produce deformed and under-sized blossoms.

As many as 15,000 nematodes may be found in one leaf of chrysanthemum (MAFF, 1969); over 300 individuals per 14 g of infested aster seeds have been recovered (Brown, 1956). Limonium sinuatum attacked by A. ritzemabosi also showed a high level of infestation, more than 100 individuals per 2.5 g foliar tissue (Bohm and Aruta, 1985).

A. ritzemabosi multiplies bisexually and not by parthenogenesis; fertilized females go on reproducing for 6 months without further fertilization (French and Barraclough, 1961). In chrysanthemum leaves, a female lays about 25-30 eggs in a compact group; eggs hatch in 3-4 days and the juveniles take 9-10 days to reach maturity; the life cycle takes 10-13 days (Wallace, 1960). In leaves of groundsel (Senecio vulgaris) the life cycle is completed in 14-15 days (Stewart, 1921). In susceptible chrysanthemum varieties the female remains in the leaf at one place, feeds on adjoining cells and lays many eggs which hatch into rapidly developing juveniles; however, in resistant varieties the female moves about rapidly through the tissues, feeding on cells, but lays only a few eggs whose emerging juveniles fail to reach maturity (Wallace, 1961).

In strawberry fields in Poland, both Aphelenchoides fragariae and A. ritzemabosi showed peak populations in March-May and November-January, and were influenced by moisture and temperature (Szczygiel and Hasior, 1972).

Like other plant-parasitic Aphelenchoides species such as A. fragariae, A. besseyi and A. blastophthorus, A. ritzemabosi can reproduce on fungi, and soil fungi may therefore contribute to its survival in the absence of a host (Hooper and Cowland, 1986).

Survival and source of infection

A. ritzemabosi survives unfavourable conditions through anhydrobiosis, as it possesses multiple contraction ability, i.e. coiling coupled with transverse and longitudinal folding of the cuticle. It survived immersion in paraffin oil for 12 days (Saeed and Roessner, 1984). Christie (1959) revived specimens in dried chrysanthemum leaves after 16 months, but not after 19 months; Steiner (1924) revived them after 22 months; Voss (1930) after 2 years; and Goodey (1933) after 3 years.

A. ritzemabosi overwinters in dormant buds and growing points of chrysanthemum stools; stools rather than the soil serve as the source of infestation (Hesling and Wallace, 1961). The nematode is also carried on the seeds of aster (Brown, 1956).

No change in nematode population per number of hearts occurred when strawberry plants infested with A. ritzemabosi and A. fragariae were stored at a room temperature of 14-15°C or in an unheated glasshouse in winter. However, at 20°C the population increased several times. Under cold-storage conditions of -2 to -1°C, an increase of 56% was registered (Hirling, 1972); at 4°C, 33% revived after 3 years (French and Barraclough, 1962).

Several weeds are hosts (goosegrass, chickweed, buttercup, sowthistle, speedwell) hence weed control is important.

Culture

A. ritzemabosi was mass cultured on courgette and/or marrow tissues at 16-18°C (Hooper and Cowland, 1988). In oat callus tissue, the nematode increased 50-fold in 6 weeks, although oat is not a recorded host (Webster, 1966); numbers increased in plant growth-stimulating substances (Webster, 1967). It also reproduced and multiplied in callus tissues of carrot, tobacco, periwinkle and marigold; the reproduction seemed to be influenced by the concentration of cations in the culture (Dolliver et al., 1962).

Monoxenic cultures of A. ritzemabosi, Ditylenchus dipsaci, Pratylenchus penetrans and Pratylenchus vulnus were obtained on lucerne and clover callus tissue by the method of Eriksson (described by Bossis and Caubel, 1982).

Interactions with other Organisms

Cross and Pitcher (1952) co-inoculated A. ritzemabosi and Corynebacterium fascians [Rhodococcus fascians] to strawberry runners and produced the 'cauliflower' disease resulting in the continued production of axillary buds on affected crown. In such an interaction, nematodes appear to act as vectors for the bacteria and may also stimulate bacterial growth either by producing a suitable metabolite or by modifying the host substrate (Pitcher, 1963). In southern regions of Russia, A. ritzemabosi and highly virulent strains of C. fascians are thought to be responsible for 'cauliflower' symptoms, and less virulent strains are thought to cause 'red plants' or 'alaminate leaves' (Drozdovski et al., 1971). The alaminate leaves condition of strawberry is due either to the nematodes alone, or to the nematodes acting in association with less virulent strains of C. fascians (Pitcher and Cross, 1958).

In experiments, population growth of Ditylenchus dipsaci on tobacco was depressed by simultaneous infection with A. ritzemabosi. The latter species was not affected by D. dipsaci in the leaves; however, in the stems and petioles, where A. ritzemabosi does not normally develop, its population growth was enhanced, possibly due to the chemical and histological changes induced by D. dipsaci (Weischer, 1974).

In tests on tobacco plants, A. ritzemabosi was inhibited by Tobacco mosaic virus, Tobacco rattle virus, Tomato ringspot virus, Raspberry ringspot virus and Tomato black ring virus, and favoured by Arabis mosaic virus. The negative or positive influence of a virus is due to the various physiological changes it causes in a plant, and not to a direct influence on the nematodes which ingest the virus particles with the cell contents (Weischer, 1969, 1975).

A. ritzemabosi was found in association with Phytophthora cryptogea on diseased gloxinia plants in Florida (Stokes and Alfieri, 1969).
 

The bulb mite Rhizoglyphus echinopus was found to feed on A. ritzemabosi (Sturhan and Hampel, 1977).

The nematode is carried on the seeds of aster (Brown, 1956). Adults and stage IV juveniles of A. ritzemabosi and Aphelenchoides blastophthorus were isolated from seeds and tissue fragments of china aster, Callistephus chinensis. The nematodes were found between the testa and embryo, the embryos remaining uninfested (Burckhardt, 1972).

Increased numbers of A. ritzemabosi and A. fragariae infesting strawberry or chrysanthemum were recovered by funnel extraction using dilute hydrogen peroxide instead of water (Hirling, 1971).

Infested chrysanthemum leaves become crinkled and deformed, occasionally accompanied by discoloration, and by nematodes in buds inhabiting mainly the axils or innermost parts of the bud (Kobayashi et al., 1971).

Infected plants of Zinnia elegans, Salvia splendens, Chrysanthemum sp., Aster sp. and Dahlia sp. had fewer and smaller leaves than healthy plants, and the leaves appeared shrunken. Yellow-white spots which gradually turned brown were observed on infected plants (Gill and Sharma, 1979). Zinnia elegans leaves infested with A. ritzemabosi showed a higher concentration of total phenols, ortho-dihydroxy phenols, total sugars and reducing sugars than uninfested leaves (Gill and Uppal, 1979).

Infestation of strawberry is generally concentrated in the buds and folded leaves within the hearts. The suspected plant tissues may be chopped up and submerged in water to see if the nematodes are present.

A. ritzemabosi occurs sympatrically with A. fragariae on 28 hosts including strawberry, aster and begonia, and on one species of fern (Struthiopteris orientalis). A. ritzemabosi mostly parasitizes members of the Compositae, whereas A. fragariae occurs mostly on ferns, Liliaceae, Primulaceae and Ranunculaceae (see Siddiqi, 1974, 1975). The two species can be differentiated using morphological characters: A. ritzemabosi can be distinguished from A. fragariae by the position of the excretory pore at 0.5-2 body widths behind the nerve ring (level with or closely behind the nerve ring in A. fragariae), the females having an irregular tail mucro and four incisures in the lateral field (tail mucro simple, spike-like, two incisures in the lateral field in A. fragariae) and the males lacking dorsal and ventral processes on the proximal end of the spicule (present in A. fragariae); longer dorsal limb of spicule (14-17 µm long in A. fragariae).

Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

Introduction

Symptoms and control of diseases in strawberry due to infestation by A. ritzemabosi and Aphelenchoides fragariae are described in an advisory leaflet (MAFF, 1970). Siddiqi (1974) reviewed control of A. ritzemabosi.

Chemical Control

On begonia spraying with demeton (superseded) and with sodium selenate gave good control (see Siddiqi, 1974).

Strawberry runners treated with fensulfothion (superseded) were less susceptible to attack than the untreated ones (Hirling, 1970).

Of the spray chemicals fenitrothion gave the best control of A. ritzemabosi (Baranowski, 1985).

Treatment of chrysanthemum nursery soil with an organophosphorous nematicide was very effective in control of this nematode (Fukazawa and Kobayashi, 1971; Kobayashi et al., 1971).

Suggested control measures include cleaning and burning infested leaves, submerging infected cuttings in hot water, spraying of foliage with chlorpyrifos (Gill, 1981). Foliar sprays of quinalphos successfully controlled A. ritzemabosi on Zinnia elegans, reducing both the symptoms of infestation and the final nematode population (Gill and Walia, 1980).

Guidelines have been given for the efficacy evaluation of nematicides against A. ritzemabosi and A. fragariae on susceptible cultivars of ornamentals such as Chrysanthemum indicum [Dendranthema indicum], Begonia elatior [B. hiemalis], Primula denticulata, Verbena hybrida, Saintpaulia ionantha or Weigela spp. (EPPO, 1994). The UK Ministry of Agriculture, Fisheries and Food's 1976 revised edition of an advisory leaflet on chrysanthemum eelworm disease caused by A. ritzemabosi emphasizes chemical control, giving instructions for the use of thionazin (superseded) and places hot-water treatment in second place. This is a reflection of the development of year-round chrysanthemums with small stools (MAFF, 1976).

Host-Plant Resistance

In Japan, 61 strawberry cultivars were studied and divided into three groups according to susceptibility to injury by A. ritzemabosi. The most resistant group contained 14 cultivars (including Otomezakuramomo), the group with medium resistance contained 32 cultivars (including Seikobizan), and the most susceptible group contained 15 cultivars (including Hagoromo) (Nakagome and Kato, 1977). In Poland, none of the 33 strawberry cultivars was entirely resistant to A. ritzemabosi and A. fragariae, but the degree of their susceptibility differed greatly. The cultivars Purpuratka, Senga Sengana, Macherauchs Fruhernte, Koralovaya and Templar were highly susceptible (Szczygiel and Danek, 1975).

Chrysanthemum varieties Amy Schoesmith, Orange Beauty and Orange Peach Blossom are comparatively resistant, but not immune (Hesling and Wallace, 1961; Wallace, 1961), as are the strawberry varieties George Soltwedel and Regina (Szczygiel, 1967). Of 20 varieties of African violet (Saintpaulia ionantha) tested in the USA, Allison and Suzanne are most resistant to the nematode, whereas Julianne, Maryland, Mitzi, Pearl and Colorado are the most susceptible varieties (Strider, 1979).

Several authors (Goffart, 1930; Voss, 1930; Wilson, 1943, etc.) have listed varieties of chrysanthemum differing in their susceptibility, but Hesling and Wallace (1960) have cautioned that the degree of nematode infestation may be considerably influenced by cultural methods, soil type and weather (see also Szczygiel, 1967). It should be noted that the commercial varieties are constantly changing and new ones are being introduced, so that a list of resistant or less-resistant varieties will not serve any practical purpose (MAFF, 1969).

Cultural Practices and Hot-Water Treatment

Cultural methods of control include thorough and constant rogueing of plants showing signs of infestation; burning all infected material; propagating only from healthy stocks and in clean soil and containers; and avoiding contact between plants and undue surface moisture of the leaves (Siddiqi, 1975). In France, cultural methods to control A. ritzemabosi, A. fragariae and other pests and diseases of strawberry include the use of healthy, well adapted cultivars; manuring based on soil analysis with special attention to boron; draining or planting on ridges to avoid waterlogging; and irrigating at planting, during the summer of planting and again in the following spring (Clerjeau et al., 1983).

Christie (1959) reported the successful use of hot-water treatment at 44.4°C for 30 min for control of A. ritzemabosi on chrysanthemum, and reported that chrysanthemum stools show good tolerance to hot-water treatment although treated plants were slower in growth. Hot-water treatment at 46°C for 10 min controlled A. ritzemabosi and A. fragariae on begonias in Denmark (Rasmussen, 1971) and on strawberry in Switzerland (Klingler, 1969). Strawberry runner initials were hot-water treated at 45 and 50°C for 10 and 15 min to control A. ritzemabosi, A. fragariae and D. dipsaci. The results showed that runner initials will tolerate 45°C for 10 min provided they are pre-heated in warm water, immersed in cold water after treatment, and planted in a frame covered with white polythene. Best results should be obtained if runners are taken before September (MacLachlan and Duggan, 1979).

Hot-water treatment at 46°C for 10 min controlled A. ritzemabosi and A. fragariae on Lorraine begonia (Rasmussen, 1971). For lily bulbs, a hot-water formaldehyde bath (1 pint of 38% formaldehyde in 25 gallons of water) at 44°C for 1 h was effective (Jensen and Caveness, 1954).

Tobacco plants inoculated with the endotrophic mycorrhizal fungus Glomus mosseae and with A. ritzemabosi showed a decrease in nematode populations by 48% 30 days after inoculation, compared to non-mycorrhizal controls (Sikora and Dehne, 1979).

Common weeds (goosegrass, chickweed, buttercup, sowthistle, speedwell) are hosts and hence weed control is important in the control of A. ritzemabosi populations.