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Datasheet

Aphelenchoides ritzemabosi
(Chrysanthemum foliar eelworm)

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Datasheet

Aphelenchoides ritzemabosi (Chrysanthemum foliar eelworm)

Summary

  • Last modified
  • 14 July 2018
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Preferred Scientific Name
  • Aphelenchoides ritzemabosi
  • Preferred Common Name
  • Chrysanthemum foliar eelworm
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Metazoa
  •     Phylum: Nematoda
  •       Order: Aphelenchida
  •         Family: Aphelenchoididae

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Pictures

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PictureTitleCaptionCopyright
All stages of A. ritzemabosi in tissues of chrysanthemum leaf.
TitleAll stages
CaptionAll stages of A. ritzemabosi in tissues of chrysanthemum leaf.
Copyright©J. Bridge/CABI BioScience
All stages of A. ritzemabosi in tissues of chrysanthemum leaf.
All stagesAll stages of A. ritzemabosi in tissues of chrysanthemum leaf.©J. Bridge/CABI BioScience
Interveinal necrosis on chrysanthemum leaves caused by A. ritzemabosi.
TitleInterveinal necrosis
CaptionInterveinal necrosis on chrysanthemum leaves caused by A. ritzemabosi.
Copyright©J. Bridge/CABI BioScience
Interveinal necrosis on chrysanthemum leaves caused by A. ritzemabosi.
Interveinal necrosisInterveinal necrosis on chrysanthemum leaves caused by A. ritzemabosi.©J. Bridge/CABI BioScience

Identity

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Preferred Scientific Name

  • Aphelenchoides ritzemabosi (Schwartz, 1911) Steiner & Buhrer, 1932

Preferred Common Name

  • Chrysanthemum foliar eelworm

Other Scientific Names

  • Aphelenchoides ribes (Taylor, 1917) Goodey, 1933
  • Aphelenchus phyllophagus Stewart, 1921
  • Aphelenchus ribes (Taylor, 1917) Goodey, 1923
  • Aphelenchus ritzema-bosi (Schwartz, 1911)
  • Pathoaphelenchus ritzemabosi (Schwartz, 1911) Steiner, 1932
  • Pseudaphelenchoides ritzemabosi (Schwartz, 1911) Drozdovski, 1967
  • Tylenchus ribes Taylor, 1917

International Common Names

  • English: chrysanthemum foliar nematode; leaf and bud nematode; leaf wilt nematode of chrysanthemum
  • Spanish: afelencoide del crisantemo; nematodos del crisantemo
  • French: anguillule des chrysanthèmes

Local Common Names

  • Denmark: bladal; chrysanthemumbladnematod
  • Finland: päivänkukkaankeroinen
  • Germany: Aelchenkrankheit der Chrysanthemen; Chrysanthemenalchen
  • Italy: anguillula dei crisantemi
  • Netherlands: Chrysantebladaaltje
  • Norway: krysantemumbladnematode
  • Sweden: krysantemumbladnematod

EPPO code

  • APLORI (Aphelenchoides ritzemabosi)

Taxonomic Tree

Top of page
  • Domain: Eukaryota
  •     Kingdom: Metazoa
  •         Phylum: Nematoda
  •             Order: Aphelenchida
  •                 Family: Aphelenchoididae
  •                     Genus: Aphelenchoides
  •                         Species: Aphelenchoides ritzemabosi

Notes on Taxonomy and Nomenclature

Top of page Aphelenchoides ritzemabosi was proposed by Schwartz in 1911, as a new species of Aphelenchus Bastian, 1865. Steiner and Buhrer (1932) transferred it to Aphelenchoides Fischer, 1894. Steiner (1932) had proposed a new genus, Pathotylenchus, to which he assigned this species as Pathotylenchus ritzemabosi. The species was later assigned to a new genus, Pseudaphelenchoides, proposed by Drozdovski (1967). Pathotylenchus and Pseudaphelenchoides were not recognized by later workers, who preferred Aphelenchoides. Two other species, proposed as Tylenchus ribes Taylor, 1917 and Aphelenchus phyllophagus Stewart, 1921, were later synonymized with A. ritzemabosi. The type host and locality of A. ritzemabosi is chrysanthemum, Redwood City, California, USA, from where the neotype was proposed by Allen (1952). The species has been assigned to the family Aphelenchidae Fuchs, 1937 and later more appropriately to Aphelenchoididae Skarbilovich, 1947.

Description

Top of page The morphology of A. ritzemabosi is described by Siddiqi (1974), Franklin and Southey (1978), Khan et al. (1987) and Hunt (1993).

Measurements (after Allen, 1952). Females: length = 0.77-1.20 mm; a = 40-45; b = 10-13; c = 18.24; V = 66-75%. Males: length = 0.70-0.93 mm; a = 31-50; b = 10-14; c = 16-30; T = 35-64%.

Body elongate-slender. Cuticle marked by transverse striae 0.9-1.0 µm apart; lateral field with four incisures. Cephalic region hemispherical, smooth, set off from body by a constriction, slightly wider than adjacent body. Stylet about 12 µm long, with minute but distinct basal knobs and sharply pointed tip. Median oesophageal bulb prominent, somewhat oval, filling body cavity, with large cuticular valvular apparatus in centre. Nerve ring about 1.5 body widths behind median bulb. Excretory pore 0.5-2 body widths posterior to nerve ring. Oesophageal glands forming a lobe extending over intestine dorsally for about 4 body widths. Tail elongate-conoid, bearing a terminal peg which has two to four tooth-like processes pointing posteriorly and giving it a paint brush-like appearance.

Female: body when relaxed becomes straight to slightly arcuate. Vulva a transverse slit, at 66-75% of body. Postvulval uterine sac more than half the vulva-anus distance, often containing sperm. Ovary single, with oocytes in multiple rows.

Male: common. Posterior region of body curved through 180 degrees. Testis single, outstretched; sperm large-sized, rounded. Spicules large and prominent, smoothly curved, rosethorn-shaped, lacking a dorsal or ventral process at proximal end; dorsal limb 20-22 µm long.

Juveniles: four juvenile stages, resembling female in general morphology but lacking genital structures.

Distribution Table

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The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Continent/Country/RegionDistributionLast ReportedOriginFirst ReportedInvasiveReferenceNotes

Asia

ChinaRestricted distributionCABI/EPPO, 2000; EPPO, 2014
-GuizhouWidespreadLi and Zhang, 1992; CABI/EPPO, 2000; EPPO, 2014
IndiaRestricted distributionGill and Sharma, 1979; Gill, 1981; CABI/EPPO, 2000; EPPO, 2014
-Himachal PradeshPresentAhmad, 1971; Khan et al., 1987; CABI/EPPO, 2000; EPPO, 2014
-Jammu and KashmirPresentKhan et al., 1987; CABI/EPPO, 2000; EPPO, 2014
IranPresentDeimi et al., 2007; EPPO, 2014
JapanRestricted distributionKobayashi et al., 1971; CABI/EPPO, 2000; EPPO, 2014
-HonshuPresentCABI/EPPO, 2000; EPPO, 2014
KazakhstanPresentCABI/EPPO, 2000; EPPO, 2014
Korea, Republic ofPresentCABI/EPPO, 2000; EPPO, 2014
UzbekistanPresentKhakimova, 1978; CABI/EPPO, 2000; EPPO, 2014

Africa

MauritiusPresentOrian, 1957; CABI/EPPO, 2000; EPPO, 2014
South AfricaWidespreadWager, 1972; CABI/EPPO, 2000; EPPO, 2014
Spain
-Canary IslandsWidespreadSturhan, 1973; CABI/EPPO, 2000; EPPO, 2014

North America

MexicoWidespreadCid del Prado & Sosa-Moss, 1978; Sandoval-Hernandez & Teliz Ortiz, 1990; CABI/EPPO, 2000; EPPO, 2014
USARestricted distributionStrider, 1979; CABI/EPPO, 2000; EPPO, 2014
-CaliforniaPresentCABI/EPPO, 2000; EPPO, 2014
-ColoradoPresentCABI/EPPO, 2000; EPPO, 2014
-FloridaPresentLehman, 1991; CABI/EPPO, 2000; EPPO, 2014
-WyomingPresentFranc et al., 1993; Franc et al., 1996; CABI/EPPO, 2000; EPPO, 2014

Central America and Caribbean

CubaPresentGandarilla Basterrechea, 2003

South America

BrazilPresentCuri and Pitta, 1971; CABI/EPPO, 2000; EPPO, 2014
-BahiaPresentCABI/EPPO, 2000; EPPO, 2014
-Sao PauloPresentCABI/EPPO, 2000; EPPO, 2014
ChilePresentBohm and Aruta, 1985; CABI/EPPO, 2000; EPPO, 2014
VenezuelaPresentMeredith and Yepez, 1973; CABI/EPPO, 2000; EPPO, 2014

Europe

BulgariaPresentSoyanov, 1975; CABI/EPPO, 2000; EPPO, 2014
CroatiaPresentPagliarini, 2006
DenmarkAbsent, formerly presentLindhardt, 1967; Andersson, 1969; Juhl, 1978; CABI/EPPO, 2000; EPPO, 2014
GermanyPresentBurckhardt, 1972; Blank, 1985; CABI/EPPO, 2000; EPPO, 2014
HungaryPresentFarkas et al., 1972; CABI/EPPO, 2000; EPPO, 2014
IrelandPresentCABI/EPPO, 2000; EPPO, 2014
ItalyPresentVovlas and Lamberti, 1973; Lamberti et al., 1987; CABI/EPPO, 2000; EPPO, 2014
LatviaPresentZvirgzdynya Zvirgzdina, 1973; CABI/EPPO, 2000; EPPO, 2014
NetherlandsPresentCABI/EPPO, 2000; EPPO, 2014
PolandPresentSzczygiel & Hasiur, 1972; Szczygiel, 1967; Szczygiel, 1970; CABI/EPPO, 2000; Cha<l>anska et al., 2014; EPPO, 2014
PortugalRestricted distributionCABI/EPPO, 2000; EPPO, 2014
-MadeiraWidespreadSturhan, 1973; CABI/EPPO, 2000; EPPO, 2014
Russian FederationPresentCABI/EPPO, 2000; EPPO, 2014
-Southern RussiaPresentCABI/EPPO, 2000; EPPO, 2014
-Western SiberiaPresentCABI/EPPO, 2000; EPPO, 2014
SerbiaPresentEPPO, 2014
SloveniaPresentUrek and ?irca, 2003
SpainRestricted distributionCABI/EPPO, 2000; EPPO, 2014
SwitzerlandPresentStaubli et al., 1989; CABI/EPPO, 2000; EPPO, 2014
UKPresentMAFF, 1970; Roberts, 1981; CABI/EPPO, 2000; EPPO, 2014
UkrainePresentLebedeva & Metliskii, 1972; Lebedeva et al., 1972; CABI/EPPO, 2000; EPPO, 2014
Yugoslavia (Serbia and Montenegro)PresentGrujicic, 1972; CABI/EPPO, 2000

Oceania

FijiPresentSwaine, 1971; CABI/EPPO, 2000; EPPO, 2014
New ZealandPresentBoesewinkel, 1980; Boesewinkel, 1982; CABI/EPPO, 2000; EPPO, 2014

Risk of Introduction

Top of page 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).

Hosts/Species Affected

Top of page 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.

Host Plants and Other Plants Affected

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Plant nameFamilyContext
Asplenium nidus (bird's nest fern)AspleniaceaeOther
BegoniaBegoniaceaeOther
Bergenia (elephant-leaved saxifrage)SaxifragaceaeOther
Buddleia (Butterflybush)LoganiaceaeWild host
Calceolaria (pouch flower)ScrophulariaceaeOther
Callistephus chinensis (China aster)AsteraceaeOther
Campanula (campanulas)CampanulaceaeOther
Campanula pyramidalis (chimney bellflower)CampanulaceaeOther
Chrysanthemum morifolium (chrysanthemum (florists'))AsteraceaeMain
Consolida ambigua (rocket larkspur)RanunculaceaeOther
Crassula coccineaCrassulaceaeOther
DahliaAsteraceaeMain
EchiumBoraginaceaeWild host
Eleusine coracana (finger millet)PoaceaeWild host
Fragaria (strawberry)RosaceaeMain
Fragaria ananassa (strawberry)RosaceaeMain
Geranium (cranesbill)GeraniaceaeOther
Helianthus annuus (sunflower)AsteraceaeOther
Helleborus niger (christmas rose)RanunculaceaeOther
Hibiscus rosa-sinensis (China-rose)MalvaceaeOther
Hydrangea anomalaOther
Lavandula angustifolia (lavender)LamiaceaeOther
Limonium sinuatum (sea pink)PlumbaginaceaeOther
Lotus corniculatus (bird's-foot trefoil)FabaceaeOther
Lupinus (lupins)FabaceaeOther
Medicago sativa (lucerne)FabaceaeOther
Mimulus (monkey-flower)ScrophulariaceaeOther
Nicotiana tabacum (tobacco)SolanaceaeOther
Ocimum basilicum (basil)LamiaceaeOther
Passiflora edulis (passionfruit)PassifloraceaeOther
PeperomiaPiperaceaeOther
Phaseolus vulgaris (common bean)FabaceaeOther
Philadelphus coronarius (mock orange)HydrangeaceaeOther
Ranunculus (Buttercup)RanunculaceaeWild host
Rheum hybridum (rhubarb)PolygonaceaeOther
Rhododendron (Azalea)EricaceaeOther
Ribes nigrum (blackcurrant)GrossulariaceaeOther
Ribes uva-crispa (gooseberry)GrossulariaceaeOther
Rudbeckia (coneflower)AsteraceaeOther
Rumex (Dock)PolygonaceaeWild host
Saintpaulia (african violet)GesneriaceaeOther
Saintpaulia ionantha (African violet)GesneriaceaeOther
Salvia splendens (scarlet sage)LamiaceaeOther
Sambucus (Elderberry)CaprifoliaceaeWild host
Senecio (Groundsel)AsteraceaeWild host
Sinningia speciosa (gloxinia)GesneriaceaeOther
Solanum lycopersicum (tomato)SolanaceaeOther
Solanum nigrum (black nightshade)SolanaceaeOther
Sonchus (Sowthistle)AsteraceaeWild host
Stellaria media (common chickweed)CaryophyllaceaeWild host
Verbena (vervain)VerbenaceaeOther
Veronica (Speedwell)ScrophulariaceaeWild host
ViburnumCaprifoliaceaeOther
Viola (violet)ViolaceaeOther
Zinnia elegans (zinnia)AsteraceaeOther

Growth Stages

Top of page Vegetative growing stage

Symptoms

Top of page A. ritzemabosi causes angular leaf spot in several hosts, and also causes dwarfing and leaf wilt.

As an endoparasite, it enters the leaves through the stomata and moves about, feeding on the mesophyll cells. The cells in infested areas are killed and the leaves develop brown lesions delimited by the veins (Franklin, 1959). Infested leaves become crinkled and deformed, occasionally accompanied by discoloration, with blotches and chlorotic patches turning into brown and white-yellow areas. The entire plant appears stunted and dwarfed.

The symptoms on chrysanthemum include characteristic brown spots limited to the veins, and a progressive yellowing of the whole leaf. These symptoms are due to combined action of the nematode and other organisms (Cayrol and Combettes, 1972). Leaf symptoms on infested Chrysanthemum maximum include reddish-yellow lesions on the lower leaves of young plants; in older plants these leaves are markedly chlorotic and a large area of the leaf surface becomes necrotic. The foliage is scanty and the flowers are few and deformed. Leaves in the upper part of plants have shown slightly higher resistance than those in the lower part (Cid del Prado and Sosa-Moss, 1978). Direct effects are mechanical damage caused by the stylet, and damage due to hormones of growth and division (Cayrol and Combettes, 1972).

Attacked violets are stunted, and affected leaves curl down, wither and die; under surfaces of leaves showed typical water-soaked blotches (Thomas, 1968). Stunting and shoot blindness occurred on attacked Crassula coccinia (Atkinson, 1964).

List of Symptoms/Signs

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SignLife StagesType
Leaves / abnormal forms
Leaves / necrotic areas
Leaves / wilting
Leaves / yellowed or dead
Stems / stunting or rosetting
Whole plant / dwarfing

Biology and Ecology

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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).
 

Natural enemies

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Natural enemyTypeLife stagesSpecificityReferencesBiological control inBiological control on
Rhizoglyphus echinopus Predator

Notes on Natural Enemies

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

Seedborne Aspects

Top of page 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).

Pathway Vectors

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VectorNotesLong DistanceLocalReferences
Clothing, footwear and possessionsWith flowers and cuttings Yes
Containers and packaging - wood Yes
Land vehicles Yes
MailWith flowers and cuttings Yes
Soil, sand and gravelWith flowers and cuttings Yes

Plant Trade

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Plant parts liable to carry the pest in trade/transportPest stagesBorne internallyBorne externallyVisibility of pest or symptoms
Bulbs/Tubers/Corms/Rhizomes adults; eggs; juveniles Yes Yes Pest or symptoms not visible to the naked eye but usually visible under light microscope
Flowers/Inflorescences/Cones/Calyx adults; eggs; juveniles Yes Yes Pest or symptoms not visible to the naked eye but usually visible under light microscope
Growing medium accompanying plants adults; eggs; juveniles Yes Pest or symptoms not visible to the naked eye but usually visible under light microscope
Leaves adults; eggs; juveniles Yes Yes Pest or symptoms not visible to the naked eye but usually visible under light microscope
Stems (above ground)/Shoots/Trunks/Branches adults; eggs; juveniles Yes Yes Pest or symptoms not visible to the naked eye but usually visible under light microscope
True seeds (inc. grain) adults; eggs; juveniles Yes Yes Pest or symptoms not visible to the naked eye but usually visible under light microscope
Plant parts not known to carry the pest in trade/transport
Bark
Fruits (inc. pods)
Roots
Seedlings/Micropropagated plants
Wood

Impact

Top of page A. ritzemabosi is a major and widespread pest of chrysanthemum in Europe, North America, South Africa, New Zealand and Australia, and chrysanthemum is regarded as the major host in Europe (Juhl, 1978; Farkas et al., 1985).

A. ritzemabosi is a serious pest of strawberry in Ireland, where yield reductions up to 60% due to A. ritzemabosi and A. fragariae infestations have been recorded (Duggan, 1969). The crown weight of strawberry cv. Senga Sengana was reduced by 51% by A. ritzemabosi and by 41% by A. fragariae. Fruit yield in the first year was reduced, owing largely to a decline in fruit number, by 65% and 54%, respectively, by these two species. The number of runners was reduced by 25-30% by A. ritzemabosi, but only by 11-15% by A. fragariae. Damage to the plant crowns and reduced yield were related to population density in winter and spring, but reduced runner production was due to the summer population density (Bohmer, 1981). Due to infection by A. ritzemabosi, average yield losses of the strawberry variety Korallovaya 100 were estimated as 53.4%. The variety Yasna seems to be somewhat less susceptible to A. ritzemabosi than Korallovaya 100 or Muto (Lebedeva et al., 1972). In Poland, A. ritzemabosi infestation destroyed 45% of chrysanthemum plants on a holding, and for the most susceptible varieties the number could be as high as 92% (Baranowski, 1976).

Diagnosis

Top of page 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).

Detection and Inspection

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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.

Similarities to Other Species/Conditions

Top of page 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).

Prevention and Control

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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.
 

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