Aphelenchoides fragariae (strawberry crimp nematode)
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- Risk of Introduction
- Hosts/Species Affected
- Host Plants and Other Plants Affected
- Growth Stages
- List of Symptoms/Signs
- Biology and Ecology
- Natural enemies
- Pathway Vectors
- Plant Trade
- Detection and Inspection
- Similarities to Other Species/Conditions
- Prevention and Control
- Distribution Maps
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IdentityTop of page
Preferred Scientific Name
- Aphelenchoides fragariae (Ritzema - Bos, 1891) Christie, 1932
Preferred Common Name
- strawberry crimp nematode
Other Scientific Names
- Aphelenchoides olesistus (Ritzema Bos, 1893) Steiner, 1932
- Aphelenchoides olesistus var. longicollis (Schwartz, 1911) Goodey, 1933
- Aphelenchoides pseudolesistus (Goodey, 1928) Goodey, 1933
- Aphelenchus fragariae Ritzema Bos, 1891
- Aphelenchus olesistus Ritzema Bos, 1893
- Aphelenchus olesistus var. longicollis Schwartz, 1911
- Aphelenchus pseudolesistus Goodey, 1928
International Common Names
- English: bud and leaf nematode; fern nematode; strawberry spring dwarf nematode
- APLOFR (Aphelenchoides fragariae)
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Metazoa
- Phylum: Nematoda
- Order: Aphelenchida
- Family: Aphelenchoididae
- Genus: Aphelenchoides
- Species: Aphelenchoides fragariae
Notes on Taxonomy and NomenclatureTop of page Aphelenchoides fragariae was proposed as a new species of Aphelenchus Bastian, 1865 by Ritzema Bos in 1891. Christie (1932) transferred it to Aphelenchoides Fischer, 1894. The species has been assigned to the family Aphelenchidae Fuchs, 1937 and later, more appropriately, to Aphelenchoididae Skarbilovich, 1947. Aphelenchoides olesistus Ritzema Bos, 1893 (Steiner, 1932) and Aphelenchoides pseudolesistus Goodey, 1928 (Goodey, 1933) are junior synonyms of Aphelenchoides fragariae. The type host and locality of A. fragariae are strawberry plants, Kent, UK. The neotype proposed and described by Allen (1952) came from strawberry in Escalon, California, USA.
DescriptionTop of page Morphology of A. fragariae is given by Allen (1952), Siddiqi (1975), Franklin and Southey (1978), Hunt (1993).
Measurements (after Allen, 1952).
Females: Length = 0.45-0.80 mm; a = 45-60 µm; b = 8-15 µm; c = 12-20 µm; V = 64-71%.
Males: Length = 0.48-65 mm; a = 46-63 µm; b = 9-11 µm; c = 16-19 µm; T = 44-61%.
Body very slender (a=45-63 µm). Cuticle marked by fine transverse striae about 0.9 µm apart; lateral field with 2 incisures appearing as a plain narrow band. Cephalic region, smooth, anteriorly flattened with straight to curved side margins, almost continuous with body contour. Stylet slender, about 10-11 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. Oesophageal glands forming a lobe extending over intestine dorsally. Nerve ring about one body width behind median bulb. Excretory pore level with or close behind nerve ring. Tail elongate-conoid, bearing a terminal peg which is simple, spike-like.
Female: Body when relaxed becomes straight to slightly arcuate ventrally. Vulva a transverse slit, at 64-71% of body. Spermatheca elongate-oval. Postvulval uterine sac more than half the vulva-anus distance, often containing sperm. Ovary single, with oocytes in a single row.
Male: Abundant. Posterior region of body curved through 45-90 degrees. Testis single, outstretched; sperm large-sized, rounded, in a row. Spicules large and prominent, smoothly curved, rosethorn-shaped, with moderately developed dorsal and ventral processes (apex and rostrum) at proximal end; dorsal limb 14-17 µm long.
Juveniles: Four juvenile stages, resembling female in general morphology but lacking genital structures.
Distribution TableTop of page
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.Last updated: 10 Jan 2020
Risk of IntroductionTop of page A. fragariae is currently targeted in regulatory programmes worldwide (O'Bannon and Esser, 1987). It is one of a group of nematodes that are presently targeted in regulatory programmes in Taiwan (Tsay, 1995). In Russia, the principal nematodes designated for quarantine measures are A. fragariae, A. ritzemabosi, Heterodera [Globodera] rostochiensis and Ditylenchus angustus (Anon., 1978).
Plant certification schemes of clean strawberry stocks can successfully control the introduction and spread of A. fragariae and A. ritzemabosi (Tacconi and Lamberti, 1994).
Quarantine checks intercepted A. fragariae on strawberry seedlings imported to Tianjin, China from the USA (Zhang and Wang, 1989).
Hosts/Species AffectedTop of page Over 250 plants in 47 families are recorded as hosts of A. fragariae (Sturhan, 1962). Some earlier records may refer to A. ritzemabosi which occurs sympatrically in about 28 hosts including strawberry, aster, begonia, etc. (Siddiqi, 1975). Hosts mostly include ferns and members of Liliaceae, Primulaceae and Ranunculaceae compared with A. ritzemabosi which mainly parasitizes members of Compositae. It has been recorded on 27 plant species in California, USA (Siddiqui et al., 1973). About 100 fern species are attacked (Sturhan, 1962; Goodey et al., 1965; Stokes, 1967a).
A. fragariae attacks above-ground parts of plants and may be endo- or ectoparasitic. In begonias, the nematode feeds on, and destroys, mesophyll cells of the leaves and may cause reddening along the veins causing the entire leaf blade to appear red; severe necrosis may result in the presence of Xanthomonas begoniae (Riedel and Larsen, 1974). Red plant symptoms are seen on strawberry var. Royal sovereign, Laxton's King George, Duke and Aberdeen Standard (Goodey, 1933).
Host Plants and Other Plants AffectedTop of page
Growth StagesTop of page Flowering stage, Vegetative growing stage
SymptomsTop of page On strawberry, A. fragariae causes malformations of the shoot such as twisting and puckering of leaves, discoloured areas with a hard and rough surface, undersized leaves with crinkled edges, reddening of petioles, short internodes of runners, reduced flower trusses with only one or two flowers and death of the crown bud (Dicker, 1948; Franklin, 1950; Iyatomi and Nishizawa, 1951; Ogilvie and Thompson, 1936). Ectoparasitic feeding on folded crown and runner buds causes small dry, brown feeding areas which can be seen on expanded leaves usually near the mid-rib; occasionally the nematodes are found in strawberry fruit pulp (Tacconi, 1972). Endoparasitic feeding within leaf tissue produces typical leaf-blotch symptoms. The strawberry disease referred to as Spring dwarf, Spring crimp and Red plant, may be due wholly or partly to A. fragariae; sometimes these symptoms could be due to other nematodes (A. ritzemabosi, Ditylenchus dipsaci) or caused by bacteria or frost.
On flowering plant leaves, the feeding areas appear as irregular, water-soaked patches later turning brown, violet or purple. Stokes (1979) describes leaf lesions and bud abnormalities on ornamental plants caused by A. fragariae in Florida, USA. The nematode causes die-back disease of lilies, in which leaves, flower buds and fruits turn brown and die. Decay of buds of tree peonies in Japan due to A. fragariae has been reported (Saigusa, 1968). Symptoms on Philippine violet (Barleria cristata) begin as chlorotic vein delineated areas which later change to light brown, then dark brown and finally black (Lehman and Miller, 1988).
In British ferneries, leaf-blotch symptoms are well marked during winter when vegetative growth is lowest (Goodey, 1933). Typical water-soaked stripes on fronds of Western Sword-fern (Polystichum munitum) are seen during February-March in Oregon, USA, and the stripes turn brown in summer when the fern forest dries out (Sandeno and Jensen, 1962). On ferns, for example, Pteris spp., leaf blotches or water-soaked areas occur in stripes, often chevron-like. It causes severe deformity of the fronds of Sphaeropteris cooperis.
List of Symptoms/SignsTop of page
|Leaves / abnormal colours|
|Leaves / abnormal forms|
|Leaves / necrotic areas|
|Whole plant / plant dead; dieback|
Biology and EcologyTop of page A. fragariae is an obligate parasite of above-ground plant parts and may be ecto- or endoparasitic. On strawberry it is ectoparasitic on folded crown and runner buds, feeding causing small, dry brown areas delimited by the midrib and major veins. The nematodes may be found feeding endoparasitically on leaf tissues and have occasionally been found in fruit pulp (Tacconi, 1972). In violets, it is also ectoparasitic in the unopened leaf and flower buds and has been found within the ovary. It is endoparasitic in leaves of ferns, begonias, peonies, etc., the feeding causing leaf-blotch symptoms. The nematode enters the leaf through the stomata when the surface is covered with a thin film of water (Klingler, 1970), or by penetrating the epidermis of the under surface (Strümpel, 1967). Both A. fragariae and A. ritzemabosi showed peak populations in March to May and November to January and were influenced by moisture and temperature (Szczygiel and Hasior, 1972).
Reproduction and life cycle
A. fragariae is bisexual and amphimictic with n=2 (A. ritzemabosi and A. besseyi are also amphimictic with n=4 and n=3, respectively) (Cayrol and Dalmasso, 1975). In the leaves of Lorraine begonia the life cycle is completed in 10-11 days at 18°C. The eggs hatch in 4 days and the juveniles mature in 6-7 days; about 32 eggs are laid by a single female (Strümpel, 1967).
The nematode cannot survive in soil without a host for more than 3 months (Szczygiel and Hasior, 1971). It survived in a dormant state in fern fronds buried in soil for at least 46 days (Stewart, 1921).
No change in nematode population per number of hearts occurred when strawberry plants infested with A. fragariae and A. ritzemabosi were stored at temperatures of 14-15°C or in an unheated glasshouse in winter. However, at 20°C, the population increased several times. Under cold-storage conditions at -2 to -1°C it performed well in plant tissues (Tacconi, 1972). Relatively few individuals of A. fragariae survived at -20°C (Hirling, 1972). Under dry conditions, A. fragariae survived in damaged lily leaves for more than 600 days (Yamada and Takakura, 1987).
Feeding on strawberry crown affects feeding areas only (Crosse and Pitcher, 1952), but when involved with the bacterium, Corynebacterium fascians, cauliflower disease symptoms were produced; the bacterium alone causes galls and secondary crowns (Pitcher and Crosse, 1958; Strümpel, 1968). In the USSR, A. fragariae and highly virulent strains of C. fascians are thought to be responsible for cauliflower symptoms and less virulent strains cause red plants or alaminate leaves (Drozdovski et al., 1971). In the Moscow region, analysis of A. fragariae-Corynebacterium fascians infection in strawberry fields showed the incidence of infection amongst plants established for 3 to 4 years to be 3 to 7 times higher than for those established for shorter periods (Matveeva and Yakubovich, 1972).
On Rieger begonias, in the presence of A. fragariae the bacterial leaf spot disease caused by Xanthomonas begoniae was more severe and developed more rapidly than when bacteria alone were present (Riedel and Larsen, 1974). A. fragariae and Pseudomonas cichorii were found interacting and causing damage on Barleria cristata in a Florida nursery. This is the first report of this association (Lehman and Miller, 1988). A. fragariae and bacteria together cause necrosis in fern fronds (Aggéry, 1935).
Natural enemiesTop of page
|Natural enemy||Type||Life stages||Specificity||References||Biological control in||Biological control on|
Pathway VectorsTop of page
Plant TradeTop of page
|Plant parts liable to carry the pest in trade/transport||Pest stages||Borne internally||Borne externally||Visibility 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|
|Seedlings/Micropropagated plants||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||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|
|Fruits (inc. pods)|
ImpactTop of page A. fragariae and A. ritzemabosi reduced yield of strawberry by up to 60% in nematode-infested areas in Ireland (Duggan, 1969). A. fragariae is involved in strawberry decline in France (Clerjeau et al., 1983).
The weight of the crown of strawberry, cv. Senga Sengana, plants was reduced by 51% by A. ritzemabosi and 41% by A. fragariae. Fruit yield in the first year was reduced, owing largely to declines in fruit number, by 65% and 54%, respectively, by the 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).
The susceptible strawberry cultivars Macherauchs frühernte and Cambridge favourite showed 65% and 82% reduction in yield, respectively, after 2 years infestation in Poland (Szczygiel, 1963)
Heavy losses of bird's-nest fern (Asplenium nidus) have been recorded in California, USA (Ark and Tompkins, 1946).
A foliar blight of anthurium (Anthurium andraeanum) in Hawaii which is often lethal in young plants was found to be caused by Aphelenchoides fragariae. The nematode also invades and destroys anthurium seeds (Hunter et al., 1974).
Detection and InspectionTop of page Leaf and bud symptoms should be examined. Look for malformations of shoots such as twisting and puckering of leaves, discoloured areas with hard and rough surfaces, undersized leaves with crinkled edges, reddening of petioles, and for strawberries, short internodes of runners, reduced flower trusses with only one or two flowers and dying crown bud. Leaf symptoms on Philippine violet (Barleria cristata) begin as chlorotic vein delineated areas which later change to light brown, then dark brown, and finally black (Lehman and Miller, 1988); dieback disease symptoms with pronounced discolouration of leaves are seen on lilies in Japan (Yamada and Takakura, 1989).
The nematode is detected by removing diseased tissues and submerging them in water for about 24 hours. The nematodes come out of the tissue into the water. Increased numbers of A. fragariae and A. ritzemabosi infesting strawberry or chrysanthemum were recovered by funnel extraction using diluted hydrogen peroxide instead of water (Hirling, 1971).
Similarities to Other Species/ConditionsTop of page Symptoms in leaves and leaf and flower buds caused by A. fragariae resemble those caused by A. ritzemabosi which may occur sympatrically with it on the same host. Leaf-blotch symptoms and the strawberry disease (Spring dwarf, Spring crimp or Red plant) symptoms may be caused wholly or partly by A. fragariae; sometimes these symptoms could be due to other nematodes (A. ritzemabosi), bacteria or frost, for example.
A. fragariae occurs sympatrically with A. ritzemabosi on 28 hosts including strawberry, aster, begonia, but only on one species of fern (Struthiopteris orientalis). The 2 species can be differentiated on morphological characters. A. fragariae can be distinguished from A. ritzemabosi by the excretory pore being situated level with or closely behind the nerve ring (at 0.5-2 body widths behind the nerve ring in A. ritzemabosi), the females having a simple spike-like tail mucro and two incisures in the lateral field (tail mucro paint brush-like, four incisures in the lateral field in A. ritzemabosi) and the males having spicules with dorsal and ventral processes at the proximal end (absent in A. ritzemabosi) and shorter dorsal limb of the spicule (dorsal limb 20-22 µm long in A. ritzemabosi). Most A. fragariae hosts belong to ferns, Liliaceae, Primulacea and Ranunculaceae, whereas those of A. ritzemabosi occur mostly in Compositae (see Siddiqi, 1974, 1975).
Prevention and ControlTop of page
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.
Symptoms and control of diseases in strawberry due to infestation by A. fragariae and A. ritzemabosi are described in an advisory leaflet (Anon., 1972a). Immersion of fresh strawberry plants in thionazin before freeze preservation virtually eliminated A. fragariae infection. Washing the plants after treatment reduced the nematicidal effect at lower concentrations (Tacconi et al., 1982).
The Hawaiian tree fern, Cobotium chamissoi, which is used as a planting medium, is the source of infection to other plants (Hunter et al., 1974).
Foliar sprays of lilies with demeton were effective (Jensen and Caveness, 1954).
Abamectin applied to Lamium maculatum foliage infested with A. fragariae significantly reduced the numbers of A. fragariae recovered, with applications at a higher rate destroying all nematodes (LaMondia, 1996).
Of over 13 varieties of strawberry tested, Saksonka [Saxon] and Festival'naya [Festival], were fairly resistant to A. fragariae (Ivanova, 1970). Among several introduced and new Soviet strawberry varieties, 11 varieties were found to be relatively resistant to A. fragariae (Naumova, 1972). In Poland, strawberry varieties George Soltwedel, Regina and Talizman are comparatively resistant (Szczygiel, 1963, 1967).
None of the 33 strawberry cultivars was entirely resistant to A. fragariae and A. ritzemabosi but the degree of their susceptibility differed greatly. Cultivars Purpuratka, Senga Sengana, Macherauchs Fruhernte, Koralovaya and Templar were highly susceptible to both the nematodes; Dixieland, Schreder's Pamiat, Ville de Paris and Guardian were susceptible to A. fragariae. Very low susceptibility to A. fragariae was shown by Georg Soltwedel and Sophia, and low susceptibility by Redgauntlet, Senga Gigana and Ottawa (Szczygiel and Danek, 1975).
Thirteen nematophagous fungi attract and feed on Ditylenchus destructor and A. fragariae (Jansson and Nordbring-Hertz, 1980).
All 5 isolates of Hirsutella rhossiliensis obtained from nematodes (Heterodera avenae from Australia, Meloidogyne javanica and Criconemella xenoplax from the USA) killed 45 to 65% of A. fragariae in 4 days (Cayrol et al., 1986).
Exposing A. fragariae, in vitro, to one Wood light lamp (wavelength 300-400 nm) resulted in 100% mortality in 7 days and with 2 wood light lamps all died in 4 days (Moussa, 1972).
Hot water treatment (HWT) of infested aerial plant parts has long been in use. HWT of strawberry runners at 47°C for 15 minutes (Strümpel, 1969) and at 46°C for 10 minutes followed by a cold plunge (Anon., 1972) has been recommended. Hot water treatments on a Californian population of A. fragariae infesting 5 strawberry cultivars (Chandler, Douglas, Fern, Pajaro and Selva) were assessed. The minimum-maximum exposure periods that killed A. fragariae without damaging the cultivars tested were 20-30 minutes at 44.4°C, 10-15 at 46.1°C, or 8-10 at 47.7°C (Qui al., 1994).
Strawberry runner initials were hot-water treated at 45°C and 50°C for 10 and 15 minutes to control A. fragariae, A. ritzemabosi and Ditylenchus dipsaci. The results showed that runner initials will tolerate 45°C for 10 minutes provided they are preheated 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).
For nematode-infested lily bulbs, hot water treatment at 45°C for 20-30 min was effective (Yamada and Takakura, 1989); for one hour at 41°C or for 6 hours at 36°C (Muller, 1966). HWT at 46°C for 10 minutes controlled A. fragariae and A. ritzemabosi on Lorraine begonia (Rasmussen, 1971). For lily bulbs a hot water formaldehyde bath at 44°C for one hour was effective (Jensen and Caveness, 1954).
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 contacts between plants and undue surface moisture of the leaves (Siddiqi, 1975). In France, cultural methods to control A. fragariae and other pests and diseases of strawberry include: the use of healthy well-adapted cvs; 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).
A. fragariae population in soil in lily fields in Japan was markedly reduced by the cultivation of non-host crops such as wheat (Yamada and Takakura, 1987).
ReferencesTop of page
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