Heterodera goettingiana (pea cyst eelworm)
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IdentityTop of page
Preferred Scientific Name
- Heterodera goettingiana Liebscher, 1892
Preferred Common Name
Other Scientific Names
- Heterodera göttingiana Liebscher 1892
International Common Names
- English: pea cyst nematode; pea root eelworm
- Spanish: heterodera del guisante
- French: anguillule a kyste du pois; nematode du pois
Local Common Names
- Denmark: Ærctecystenematod
- Germany: Aelchen, Erbsen-; Aelchen, Erbsenzysten-
- Italy: anguillula del pisello
- Netherlands: erwtecystenaaltje
- Norway: ertecystenematode
- Sweden: Ärtcystnematod
- HETDGO (Heterodera goettingiana)
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Metazoa
- Phylum: Nematoda
- Order: Tylenchida
- Family: Heteroderidae
- Genus: Heterodera
- Species: Heterodera goettingiana
Notes on Taxonomy and NomenclatureTop of page
The species Heterodera goettingiana was first reported by Liebscher (1890) who referred to it as Heterodera schachtii pea strain. The cyst nematode caused crop losses in peas at the Agricultural Institute at Göttingen in Germany. Two years later, after making comparative studies on H. schachtii (already known and described from sugarbeet (Schmidt, 1871) ) and the oat cyst nematode (known at that time but not formally described as H. avenae until Wollenweber (1924) ), Liebscher (1892) described H. göttingiana and its host symptoms. The accepted spelling is now H. goettingiana.
The type site is no longer available and a neotype cyst was designated by Stone and Course (1974). The cyst was produced in soil taken from the type site and supplied by B. Weischer. The neotype slide is held in the International Type Nematology Slide Collection at IACR-Rothamsted, Harpenden, Herts., England, Type Slide no. 76/2/1.
DescriptionTop of page
Eggs are contained within the dead body of the female, the cuticle of which tans to a light and then darker brown colour to form the cyst. They may also be deposited into the soil, particularly on the surface of infected host roots, by the partly exposed, fertilized females while the females are still alive. The eggs are laid in a gelatinous matrix often referred to as an egg sac. These eggs in the sac and those within the cyst are the same size. It is possible that second stage juveniles will hatch from the egg sac before encysted eggs do. They can persist in the soil for some months and may not hatch until a new host is available.
J2 (n=50):L 486±22 µm; body width at excretory pore 19.4±0.7 µm; stylet length 24.6±0.8 µm; Stylet base to dorsal oesophageal gland duct 5.3±0.7 µm; head tip to median bulb valve 70.3±2.3 µm; head tip to excretory pore 101.6±4 µm; anus to terminus 60.1±5.3 µm; tail width at anus 12.7±0.9 µm; hyaline part of tail 37.0±3.2 µm.
The first stage juveniles moult within the egg to become the infective second stage juveniles, which remain folded three times within the egg until stimulated to hatch. The second stage juvenile is worm-like with a regularly annulated cuticle. There are three bands in the lateral field at the mid-body and, using a light microscope, magnified x 100 they appear unareolated. The head is offset, bearing two or three head annules and, as in the male, the head skeleton is hexaradiate with strong sclerotization. The cephalids are located at the level of the second and eighth annules from the head. The well developed stylet has rounded to moderately hook-shaped knobs. The oesophageal glands are extended beyond the excretory pore for about a third of the body length, from the head. The dorsal and subventral oesophageal glands, the former with prominent nucleus and latter with obscure nuclei, are similar to the glands seen in the male. The nerve ring encircles the oesophagus between the gland lobes and median bulb. The hemizonid is located one annule anterior to the excretory pore and is itself two annules long. The hemizonion is found six to eight annules posterior to the excretory pore and is less than one annule in length. About half way along the body the two-celled, genital primordium can be seen very distinctly. The tail tapers to a rounded point, the hyaline (clear) portion of which is equal to about two thirds of the tail length and often displays one or two refractive bodies near the terminus. Their function is unknown. The length of the clear or hyaline portion of the tail multiplied by the stylet length gives a helpful diagnostic value for this group.
(n=25) Stylet length 25.7±1 µm; stylet base to dorsal oesophageal gland duct 5.5±1.1 µm; number of head annules 1-3; head tip to median valve 71.8±8.4 µm; diameter of median bulb 32.7±2.3 µm; head tip to excretory pore 131.1±20.4 µm.
The female has a swollen, lemon-shaped body approximately 500 µm long and about 400 µm wide. The head at the anterior end of the body has one to three annules. The head skeleton is hexaradiate, but weak. The stylet is ca 26 µm in length. The conus represents 50% of the stylet length and the basal knobs are rounded in shape. The excretory pore is positioned at the base of the neck. The median oesophageal bulb is sub-spherical to spherical with a prominent valve. The oesophageal glands are often displaced by the large well developed ovaries. The vulva is positioned at the terminal end of the female vulval cone. The fenestral area is thin walled and crossing this transversely is the vulval bridge, which bears the vulval slit through which the eggs are extruded into an egg sac. The vulval bridge bisects the fenestra to form two almost equally sized semi-fenestrae, this whole area being bounded by a thick cuticular band. The anus lies dorsally to the bridge. Young females are white, without a yellow phase, and after a short time the female dies to form a tanned cyst.
(n=25) Length excluding neck 521±53 µm; maximum width 372±44 µm; length of fenestra 35.3±5.9 µm; width of fenestra 37.4±4.3 µm; length of semi-fenestra 16.3±3.9 µm; anus to fenestral edge 36.2±4.6 µm; length of vulval bridge 33.0±5.4 µm; maximum width of vulval bridge 3.0±0.9 µm; length of vulval slit 39.9±7.2 µm; length of underbridge 117.3±13.1 µm; maximum width of underbridge 6.1±1.5 µm.
Neotype cyst cone: Length of fenestra 35 µm; length of semi-fenestrae 15 µm and 16 µm; width of fenestra 37 µm; anus to fenestral edge 30 µm; length of vulval bridge 36 µm; maximum width of vulval bridge 5 µm; length of vulval slit 36 µm; length of underbridge 125 µm; maximum width of underbridge 5µm.
The cyst has a toughened cuticle and, although dead, has a similar shape to the female. The cyst contains viable eggs which become the infective second stage juveniles. The head is usually broken off leaving just the neck or a hole at the anterior end of the body. The terminal end of the vulval cone, unless the cyst is very old, is usually intact and is useful in the diagnosis of the Heterodera genus. H. goettingiana is ambifenestrate, i.e. it has two closely depressed semi-fenestrae as described for the female. Lateral muscles on the inner cuticle wall may be seen under the vulval bridge. In H. goettingiana this structure, the underbridge is very light and difficult to see. It is often absent from old cysts and is sometimes lost during careless preparation. Bullae (highly pigmented bodies which can be seen above or below the underbridge in other Heterodera spp.), another diagnostic feature used for the identification of cysts, are not usually present. The cuticle of the cyst is covered by ridges and folds. In H. goettingiana these form a fairly characteristic brick-work pattern around the cone and body wall. New cysts have a sub-crystalline layer, which is common in many newly formed Heterodera cysts.
(n=50) Length 1270±112 µm; width at excretory pore 24.7±0.8 µm; stylet length 26.8±1 µm; stylet base to dorsal oesophageal gland duct 7.9±1.2 µm; head tip to median bulb valve 100.9±5.5 µm; head tip to excretory pore 157.5±9.9 µm; spicule length along axis = 26.5±4.3 µm; gubernaculum length 12.2±2 µm; length of testis plus vas deferens = 663±81 µm; tail length = 5.1±1 µm.
Males are vermiform and are usually about 1300 µm in length. The tail region is short, blunt and without a bursa. On death, the male acquires a 90° twist from the mid-body to the tail along the length of the nematode. This is a characteristic of male Heterodera and Globodera. There are four incisures in the lateral fields, which are areolated, as shown by scanning electron microscopy. The head is offset and has five or six head annules. The heavily sclerotized head skeleton is hexaradiate. The cephalids are located anteriorly at the second body annule level and more posteriorly at the eighth body annule. The stylet is strong and well developed with knobs that have rounded anterior faces. The median bulb is ellipsoid with strong crescentic valves. The dorsal and sub-ventral oesophageal glands extend past the excretory pore, the sub-ventral gland lobe being the longer of the two glands. From the head end, these glands stretch to ca 15% of body length. There is a prominent dorsal gland nucleus, whereas the subventral nuclei are obscure. The nerve ring is located between the median bulb and gland lobes, surrounding the oesophagus. The hemizonid is found five or six annules in front of the excretory pore and is itself two annules in length. A hemizonion is not found. The single testis contains an abundance of round spermatogonia and is about half the total body length, ending in the vas deferens which is glandular walled with a narrow lumen. The cloacal opening is small, surrounded by a circular ring of muscle tissue. The spicules are typical of Heterodera males. Spicule tips are broad with bidentate tips (Clark et al., 1973). There is a simple rod-like gubernaculum. Phasmids and caudalids are not found.
Some measurements from other sources can be found in Franklin (1949); Hesling (1965); Behrens (1971); Mulvey (1972); Wouts and Weischer (1977); Baldwin and Mundo-Ocampo (1991); Di Vito (1991).
DistributionTop of page
H. goettingiana is widespread in Europe and Mediterranean regions. In the USA, Thorne (1961) identified a large number of H. goettingiana cysts from sweet peas (Lathyrus odoratus) growing in a glasshouse in Illinois. A similar incidence was reported from Idaho. Only recently has H. goettingiana been recorded from roots of peas grown in a number of fields in western Washington. The USA had not been known to have problems of infestation in commercial pea crops until this time (Handoo et al., 1994).
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.
|Country||Distribution||Last Reported||Origin||First Reported||Invasive||References||Notes|
|China||Present||Liu & Li, 1989; CABI/EPPO, 2003; EPPO, 2014|
|-Jiangsu||Present||CABI/EPPO, 2003; EPPO, 2014|
|Iran||Present||Maafi et al., 2004|
|Israel||Present, few occurrences||Cohn et al., 1973; CABI/EPPO, 2003; EPPO, 2014|
|Japan||Present||CABI/EPPO, 2003; EPPO, 2014|
|Jordan||Present||Bridge, 1978; CABI/EPPO, 2003; EPPO, 2014|
|Turkey||Present||CABI/EPPO, 2003; EPPO, 2014|
|Algeria||Present||Lamberti et al., 1975; CABI/EPPO, 2003; EPPO, 2014|
|USA||Present, few occurrences||Handoo et al., 1994; Thorne, 1961; CABI/EPPO, 2003; EPPO, 2014|
|-Idaho||Restricted distribution||Thorne, 1961; CABI/EPPO, 2003; EPPO, 2014|
|-Illinois||Restricted distribution||Thorne, 1961; CABI/EPPO, 2003; EPPO, 2014|
|-Pennsylvania||Restricted distribution||CABI/EPPO, 2003; EPPO, 2014|
|-Washington||Present||Handoo et al., 1994; CABI/EPPO, 2003; EPPO, 2014|
|Belgium||Present||D'Herde, 1966; CABI/EPPO, 2003; EPPO, 2014|
|Bulgaria||Present||Stoyanov, 1977; CABI/EPPO, 2003; EPPO, 2014|
|Former USSR||Present||Kirjanova & Krall, 1971|
|France||Present||Capus, 1917; Cayrol, 1961; CABI/EPPO, 2003; EPPO, 2014|
|Germany||Present||Goffart, 1941; CABI/EPPO, 2003; EPPO, 2014|
|Italy||Present||Garofalo, 1964; CABI/EPPO, 2003; EPPO, 2014|
|-Sicily||Present||Lombardo et al., 2011; Marinari-Palmisano & Cavalli, 1982|
|Malta||Present||Lamberti & Dandria, 1979; CABI/EPPO, 2003; EPPO, 2014|
|Netherlands||Present||CABI/EPPO, 2003; EPPO, 2014|
|Poland||Widespread||Brzeski et al., 1973; CABI/EPPO, 2003; EPPO, 2014|
|Portugal||Present||Macara, 1963; CABI/EPPO, 2003; EPPO, 2014|
|Russian Federation||Present||CABI/EPPO, 2003; EPPO, 2014|
|-Central Russia||Present||CABI/EPPO, 2003; EPPO, 2014|
|Slovenia||Present||CABI/EPPO, 2003; EPPO, 2014|
|Spain||Widespread||CABI/EPPO, 2003; EPPO, 2014; Tobar Jimenez, 1962|
|UK||Present||Brown, 1958; Jones, 1965; CABI/EPPO, 2003; EPPO, 2014|
|Ukraine||Present||CABI/EPPO, 2003; EPPO, 2014|
Hosts/Species AffectedTop of page
Heterodera goettingiana is a parasite of Fabaceae.
Many cultivars of Pisum sativum are recorded as susceptible. In glasshouse trials P. abyssinicum accessions MG101791, MG101793, MG101788, MG101789 and MG101790, P. elatius accession MG100956 and P. sativum var. arvense accession MG101877, appeared to show some resistance to H. goettingiana (Vito and Perrino, 1978).
Broad bean and field bean cultivars are not as seriously affected as peas when attacked by H. goettingiana and only succumb to high levels of infestation (MAFF, 1983).
Growth StagesTop of page
Seedling stage, Vegetative growing stage
SymptomsTop of page
Heterodera goettingiana becomes noticeable in infested fields when localized patches of plants become stunted and yellowed. Heavily infected pea plants are severely stunted, chlorotic and die off before the pods are full of peas. The roots of heavily infected plants are devoid of Rhizobium nodules and the root systems are smaller than those of their healthy counterparts.
The yellowing patches may expand during the growing season. This is due to the slower development of symptoms in the less heavily infected plants at the edges of the patches and not to a sudden spread of the nematodes. In general, patches in fields will increase slowly in size unless the nematode is moved during cultivation operations. When peas are grown in a monocrop in an infested field the crop will eventually fail to give an economic yield.
Symptoms ListTop of page
|yellowed or dead|
|reduced root system|
|plant dead; dieback|
Biology and EcologyTop of page
The life history and biology of most Heterodera species follow similar basic patterns. This has been shown and discussed by Macara (1963), Stone and Course (1974) and Di Vito and Greco (1986). The egg contains the first stage juvenile which moults within the egg and the second stage juvenile emerges. The second stage juvenile probably hatches in response to an environmental stimulus such as temperature. The optimum temperature for hatching is around 15°C . At temperatures greater than 25°C hatching is suppressed (Di Vito and Greco, 1986). The stimulation to hatch is also greatly influenced by root exudates from host roots (Shepherd, 1963). Older host roots seem to induce a greater rate of hatching than younger roots (Perry et al., 1980). Once the second stage juvenile has entered the host roots it will pass through three more consecutive moults to become an adult. Beane and Perry (1984) found that a temperature of 4.4°C appeared to be the basal temperature for development. Below 4.4°C the fourth stage moult is inhibited. Males are common and their development is possibly environmentally influenced, particularly at high population densities when a larger proportion of males are formed (Guevara-Benitez et al., 1970). Males begin to emerge from the host 2 months or less after juvenile invasion but maximum numbers of males emerge ca 4-4.5 months after invasion. Females enlarge in the host root tissue and eventually become so large that they break through the cortical root cells to become exposed on the root surface and are subsequently mated by males. As with other Heterodera males, they are thought not to feed but to mate and die within 2 or 3 weeks of emergence. The white female, once mated, begins to tan, there is no yellow female phase (Thorne, 1961). In optimum conditions, i.e. the correct soil moisture, a good host and a soil temperature of around 13-15°C , maximum egg production should take place and an egg sac may be present. An egg sac usually contains ca 100 eggs. In unfavourable conditions no egg sac will be produced. The number of generations produced in a year is governed by environmental factors: in the warm climates of southern Italy three generations have been recorded per year (Di Vito et al., 1974) whereas in Britain only one, and exceptionally two generations will be produced annually (Jones, 1950). Cysts can remain in fields for up to 12 years (Di Vito and Greco, 1986), still containing viable eggs.
Histological details of H. goettingiana infestations in host roots are now becoming better understood, particularly through the work of Arrigoni et al. (1981) and Melillo et al. (1990, 1992). Other workers (Endo, 1986; Wyss and Zunke, 1986) have looked at similar systems to those studied in other species of cyst nematodes such as H. glycines and H. schachtii; for example the granules released in stylet exudates and the overall changes caused in plant cells and syncytia.
Unusually, plant roots infected with H. goettingiana do not display excessive numbers of lateral rootlets. This nematode is capable of eliminating Rhizobium nodules from peas completely. In such cases, plants show severe nitrogen deficiency, chlorosis, dwarfing, limitation of the number of flowering nodes and early senescence (Oostenbrink, 1955; Perry and Beane, 1983). Extra fertilizer will not stimulate plant growth after invasion by H. goettingiana (Green and Williamson, 1978).
In the very early years of nematology, Capus (1917) noticed that the fungus Fusarium oxysporum, which often appeared alongside H. goettingiana in the field, aggravated the damage to field crops: peas would often succumb to root rot.
Nematode population densities and effects on plant yield are both variable. Winslow (1955) found that 127 eggs/gram of soil caused complete crop failure. Various other figures have been given (Winslow, 1955; Di Vito, 1978). Even in the absence of a host plant, cysts are known to remain in the soil for up to 12 years (Brown, 1958), although each year, the viability of the cyst contents falls.
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; cysts; juveniles||Yes||Yes||Pest or symptoms not visible to the naked eye but usually visible under light microscope|
|Growing medium accompanying plants||adults; cysts; juveniles||No||Yes||Pest or symptoms not visible to the naked eye but usually visible under light microscope|
|Roots||adults; cysts; juveniles||Yes||Yes|
|Seedlings, Micropropagated plants||adults; cysts; 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; cysts; 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|
|Flowers, Inflorescences, Cones, Calyx|
|Fruits (inc. pods)|
|True seeds (inc. grain)|
Similarities to Other Species/ConditionsTop of page
H. goettingiana has many similarities with other cyst nematodes, particularly those that also belong to Mulvey's Group Five, such as H. cruciferae, H. carotae and H. elachista. There are at the present time 26 known members of this group. The general structure of the vulval cone in the group, the host when known, and juvenile measurements are all critical if a correct diagnosis is to be made. The use of IEF electrophoresis for distinguishing Heterodera spp. is useful, but not everyone has the facilities for this method and it is best to use conventional means of identification as well as newer techniques to make accurate diagnosis. Cyst nematodes from other genera are easily ruled out, i.e. Punctodera, Globodera and Cactodera, and other Heterodera spp. should also be easily distinguished by their morphology.
Prevention and ControlTop of page
Control is difficult as the hatching of H. goettingiana is slow and probably takes place over several weeks (MAFF, 1983). The host will also influence how many new cysts are produced. Peas are very susceptible being adversely affected by densities as low as 0.5 eggs per g of soil (Greco et al., 1991), whilst white beans are more tolerant. As noted earlier (see Biology and Ecology), soil temperature can play a major role. In optimum conditions in Mediterranean regions, three generations with full egg sacs may be produced on a good host (Di Vito et al., 1974; Greco et al., 1986).
Vertical distribution of H. goettingiana is uncommon below a depth of 20 cm in soil (Whitehead, 1977). Crop rotation is an option in which growing non-host crops for 3-6 years can usefully lower population densities (Di Vito and Greco, 1986). It is also important to clear leguminous weeds from fields as they can act as alternative hosts. In countries with hot climates solarization may be used as a method of control. The most effective way of controlling infestations is probably by the use of resistant plants, but they are often less agronomically acceptable and only a few resistant cultivars exist (Vito et al., 1994). Workers in Jiangsu Province, China, have used resistant soybeans together with a nematicide to produce good yields in spite of the presence of H. goettingiana (Liu and Li, 1989).
In Munster, Germany, a Pasteuria isolate (HGP) found in H. goettingiana resembles three other Pasteuria species parasitizing other nematodes. All stages of Pasteuria up to the immature sporangia can be found in second stage juveniles (Sturhan et al., 1994). Females and cysts were not affected by the Pasteuria spores and males have only been rarely observed with spores attached to their cuticle (Winkelheide and Sturhan, 1993). Pasteuria was found to attack 93% of all free juveniles in soil in field studies (Winkelheide and Sturhan, 1993).
Measures are the same for most types of plant parasitic nematode. In fields where an infestation is already recognised, movement of machinery, lorries, workers, etc, must be restricted and all articles contaminated by soil, for example workers' boots, thoroughly cleaned. Transport and disposal of infested soil and plant material must be conducted in an appropriate manner. This is a particular problem in the farming of peas, especially those for the frozen market, as they are harvested by contractors who move quickly from field to field.
ReferencesTop of page
Arrigoni O, Zacheo G, Bleve-Zacheo T, Arrigoni-Liso R, Lamberti F, 1981. Changes of superoxidedismutase and peroxidase activities in pea roots infested by Heterodera goettingiana. Nematologia Mediterranea, 9(2):189-195.
Baldwin JG, Mundo-Ocampo M, 1991. Heteroderinae, cyst and non-cyst forming nematodes. In: Nickle WR, ed. Manual of Agricultural Nematology. New York, USA: Marcel Dekker, 275-362.
Beane J, Perry RN, 1984. Observations on the invasion and development of the pea cyst nematode Heterodera goettingiana in winter field beans (Vicia faba). Annals of Applied Biology, 105(3):503-508.
Behrens E, 1975. Taxonomically useful characters for the differentiation of Heterodera species. Probleme der Phytonematologie. Vortrage anlasslich der 10 Tagung uber Probleme der Phytonematologie im Institut fur Pflanzenzuchtung Gross-Lusewitz der Deutschen Akademie der Landwirtschaftswissenschaften zu Berlin am 11 Juni 1971., 122-142.
Bridge J, 1978. Plant nematology in Jordan. (ODM Report on the visit to Jordan, 3-15 April 1978.). Ascot, Berks, UK: Ministry for Overseas Development, [ii] + 20 pp.
Brown EB, 1958. Pea root eelworm in the eastern counties of England. Nematologica, 3:257-268.
Brzeski MW, D'Errico FP, Glaba B, 1973. On the occurrence of Heterodera goettingiana Leib. Materialy Ogolnopolskiego Zjazdu Warzywniczego, Skierniewice, June 14-15, 1973., 71.
CABI/EPPO, 2003. Heterodera goettingiana. Distribution Maps of Plant Diseases, No. 896. Wallingford, UK: CAB International.
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Di Vito M, Lamberti F, Greco N, 1974. The life cycle of Heterodera goettingiana Liebscher under field conditions in Southern Italy (Abstract). Proceedings of the XII International Symposium of Nematology in Europe.
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Liebscher G, 1892. Beobachtungen über das Auftreten eines Nematoden an Erbsen. Journal für Landwirtschaft, 40:357-368.
Liu J, Li QD, 1989. Occurrence, host resistance and chemical control of the pea cyst nematode [Heterodera goettingiana] on soyabeans (Glycine max.) in Jiangsu province. Jiangsu Agricultural Sciences, No. 6, 24-25.
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- = Present, no further details
- = Evidence of pathogen
- = Widespread
- = Last reported
- = Localised
- = Presence unconfirmed
- = Confined and subject to quarantine
- = See regional map for distribution within the country
- = Occasional or few reports