Rev 10/20/2023
Tylenchida Tylenchina Tylenchoidea Heteroderidae Heteroderinae
Heterodera trifolii Goffart, 1932
A member of the Schachtii group of Heterodsera spp.
Synonyms: Heterodera shachtii var. trifolii (Goffart, 1932)
Heterodera trifolii trifolii (Goffart, 1944)
Heterodera (Heterodera) trifolii (Skarbilovich, 1959)
General Characteristics of the Schachtii Group of Heterodera
Cysts lemon-shaped Ambifenestrate Bullae well-developed Underbridge well-developed vulval slit long J2 incisures 4 Dicotyledonous hosts
(Handoo and Subbotin, 2018; Subbotin et al., 2010, Subbotin et al. 2023)
Lip region set off from neck, rounded, with 6 annules.
Stylet well-developed with knobs slightly backward sloping.
Esophageal glands less well-developed than in infective second-stage juvenile.
Excretory pore posterior to esophago-intestinal valve. The is hemizonid 6 to 14 annules in from of the excretory pore (Norton 1967).
Testis single; spicule curved, blades with truncated or oblique lips, not appearing bidentate. Gubernaculum simple, proximity arcuate. According to Norton (1967), the spicules appear to be bidentate.
Second-stage Juvenile: Head offset, with 4 annules, head skeleton heavily sclerotized.
Stylet robust, anterior surfaces of knobs concave.
Dorsal gland duct opening 5-9 um posterior to spear knobs. Esophageal glands, particularly the subventrals, well-developed, extending ventrally or ventro-laterally well posterior to esophago-intestinal valve.
Tail conoid, tapering uniformly to a finely rounded terminus. Posterior half of tail hyaline. Phasmids small, usually obscure, located near middle of tail.
Median esophageal bulb rounded, with distinct valve.
Ovaries paired, greatly extended and nearly filling the body cavity of the adult female.
Vulval cone covered with a gelatinous matrix containing as many as 200 eggs (Thorne, 1961).
Surface of female and newly-formed cysts typically encrusted with a material termed "subcrystalline layer." Transitional stage between white female and brown cyst distinctly yellow. The yellow color varies with the strain of the host plant, being constant in females developing on any one host strain (Norton, 1967).
Cyst: Brown to dark brown containing a few to several hundred eggs, eventually becoming detached from the roots to lie in the soil where the protected eggs may remain viable for several years.
Identification of species of Heterodera is based largely on the cone top structures, including fenestra (thin-walled areas around the gonopore of the cyst), vulval slit length, underbridge and bullae (see Mulvey, 1972).
H. trifolii can be separated from H. trifolii by its heavier and more strongly pigmented underbridge, with bifurcate ends, its greater fenestral length, and shorter vulva-anus distance.
H. trifolli is considered to be in the Schachtii group of cyst nematodes (Subbotin et al., 2010).
Reported median body size for this species (Length mm; width micrometers; weight micrograms) - Click:
Cosmopolitan species, occurring widely throughout northern Europe and Spain, Italy, southern France, Soviet Union, Canada, U.S., Israel, India, Australia and New Zealand.
In California, H. trifolii was first reported by Raski and Hart (1953) from white clover in the lawn of a private residence in Camarillo, Ventura County. Due to its former D-rating in the state, the distribution of this nematode in California probably has not been well-documented (Scheck, 2023)
C-rated pest in California Nematode Pest Rating System; Transferred from D-rated to C-rated, August, 2023 (Scheck, 2023).
Feeding site establishment and development typical of genus.
Hosts of the Schachtii group of Heterodera spp. are usually dicotyledonous plants. Attacks legumes (86 species in 9 families). Several forms of clover are reported as hosts of H. trifolii in New Zealand (Mercer and Woodfield, 1986). A species thought to be H. trifolii is a serious pest of carnation in Italy and in glasshouses in southern France.
Ecophysiological Parameters:
There may be several pathotypes of H. trifolii.
Root leachates stimulate hatching and attract juveniles to root-tips.
Probably triploid, 3n=27 (although 26 and 28 chromosomes have been reported). Males are rarely reported; reproduction is by parthenogenesis.
Females are sedntary endoparasites; at maturity, the posterior of the body protrudes from the root.Eggs are produced early by the adult white female; the first eggs are laid in a gelatinous matrix adhering to the vulval cone. Most eggs, however, mature within the extensive gonad as the cyst develops, and are retained within the brown cyst.
First-stage juveniles molt to the second, infective stage within the egg. Hatching of the eggs retained within the protective cyst, however, occurs progressively over a period of years in the soil in response to moisture and root leachates. Emergence from juveniles in cysts may be seasonal and influenced by diapause and temperature. Juveniles emerge over a relatively wide range of temperatures (4.2 to 31.4 C), with 17.2 C being optimum (Oostenbrink, 1967).
Multiple infections may kill root tip.
Freckman & Chapman (1972) showed that, with mixed infestations of H. trifolii and M. hapla), syncytia and giant cells occurred side-by-side with no interference.
Aboveground symptoms of damage by H. trifolii are non-specific; there may be chlorosis, with leaves first appearing yellowish red and then turning necrotic in older parts, stunted growth, or wilted plants. In fields, poor and patchy plant growth is apparent in circular areas. Below ground there may be abnormally branching rootlets stimulated near the point of infection, a general debilitation and reduction in the efficiency of the root system (Chitambar et al., 2018; Scheck, 2023)..
Methods for controlling other species of Heterodera are generally applicable for this species, although seldom employed.
Resistance is known in some white clovers (Kuiper, 1960) and soybeans (Mankau & Linford, 1956).
Endo & Schaeffer (1967) discovered that applications of the chemical azauracil consistently arrested further development of early third-stage juveniles in red clover under greenhouse conditions.
Nematicides: In France, also in greenhouses, Aldicarb applied in November and February at doses of 45, 7.5 or 19 kg a.i./ha, resulted in reduced infestation and increased flower yield in carnation nurseries (Cuany, 1970).
The occurrence of the cysts on weed species can be a source of inoculum for susceptible species (Nunez-Rodr�guez et. al., 2021
Chitambar, J. J., Westerdahl, B. B., and Subbotin, S. A. 2018. Plant Parasitic Nematodes in California Agriculture. In Subbotin, S., Chitambar J., (eds) Plant Parasitic Nematodes in Sustainable Agriculture of North America. Sustainability in Plant and Crop Protection. Springer, Cham.
Kuiper, K. 1960. Resistance of white clover varieties to the clover cyst eelworm Heterodera trifolii Goffart Nematologoica 5 (Suppl. 11):95-96.
Mankau, R. and Linford, M.B. 1960. Host-parasite relationships of the clover cyst nematode Heterodera trifolii Goffart Bull. Illinois Ag Expt. Sta. 667:1-50.
Endo, B.Y., Schaeffer, G.W. 1967, Response of Heterodera trifolii in red dlover roots to Azauracil and other inhibitors. Phytopathology 57:576-579.
Freckman, D.W., Chapman, R.A. 1972. Infection of red clover seedlings by Heterodera trifolii Goffart and Pratylenchus penetrans Cobb. J. Nematology 2:23-28.
Goffart, H. 1932. Untersuchungen am Hafernematoden Heterodera schachtii Schm. unter besonderer Ber�cksichtigung der schlewigholsteinischen Verh�ltnisse. I. III. Beitrag zu: Rassenstudien an Heterodera schachtii Schm. Arbeiten aus der Biologischen Reichsanstalt, Berlin 20, 1-26.
Handoo, Z.A., Subbotin, S.A. 2018. Taxonomy, identification and principal species. Chapter 15 in Perry, R.N. Moens, M., and Jones, J.T.(eds) Cyst Nematodes. CAB International.
Mercer, C.F. and D.R. Woodfield, 1986. A survey of root knot and clover cyst nematodes in dry hill country. Proc. NZ Grassland Assoc. 47:267-271.
Mulvey, R.H. 1972. Identification of Heterodera cysts by terminal and cone top structures. Can. J. Zool. 50:1277-1292.
Mulvey, R.H., Anderson, R.V. 1972. CIH Descriptions of Plant-parasitic Nematodes, Set 4, No. 46 (1972)
Norton, D.C. 1967. Relatioships of Heterodera trifolii to some forage legumes. Phytopathology 57:1305-1308..
Nunez-Rodr�guez, L.A., Flores-Chaves, L. and Humphreys-Pereira, D.A., 2021. First report of Heterodera trifolii on white clover and Rumex obtusifolius in Costa Rica. Plant Disease, 105(1), p.230.
Oostenbrink, M. 1967. Studies on the emergence of encysted Heterodera larvae. Meded. Rijksfac. Landbw. Ghent. 32:503-509..
Raski, D.J. and Hart, W.H., 1953. Observations on the clover root nematode in California. Plant Disease Reporter, 37(4), pp.197-200.
Scheck, H.J. 2023.California Pest Rating Proposal for Heterodera trifolii Goffart,1932 clover cyst nematode. CDFA, Sacramento, California, USA.
Subbotin, S,A., Mundo-Ocampo, M., Baldwin, J.G. 2010. Systematics of Cyst Nematodes (Nematode: Heteroderinae). Nematology Monographs and Perspectives Volume 8B, D.J. Hunt and R.N. Perry (eds) Brill, Leiden, The Netherlands 512p
Subbotin, S.A., Roubtsova, T.V., Bostock, R.M., Maafi, Z.T., Chizhov, V.N., Palomares-Rius, J.E., Pablo Castillo, P. 2023. DNA barcoding, phylogeny and phylogeography of the cyst nematode species of the Schachtii group from the genus Heterodera (Tylenchida: Heteroderidae). Nematology (in press).