Control of Meloidogyne javanica by Formulations of Inula viscosa
Yuji Oka,1Bat-Hen Ben-Daniel,2Yigal Cohen3
Abstract: Inula viscosa is a perennial plant that is widely distributed in Mediterranean countries. Formulations of I. viscosa extracts
were tested for their effectiveness in control of Meloidogyne javanica in laboratory, growth chamber, microplot, and field experiments.
Oily pastes were obtained by extraction of dry leaves with a mixture of acetone and n-hexane or n-hexane alone, followed by
evaporation of the solvents. Emulsifiable concentrate formulations of the pastes killed M. javanica juveniles in sand at a concen-
tration of 0.01% (paste, w/w) or greater and reduced the galling index of cucumber seedlings as well as the galling index and
numbers of nematode eggs on tomato plants in growth chamber experiments. In microplot experiments, the hexane-extract
formulation at 26 g paste/m2reduced nematode infection on tomato plants in one of two experiments. In a field experiment, a
reduction of 40% in root galling index by one of two formulations was observed on lettuce plants. The plant extracts have potential
as a natural nematicide, although the formulations need improvement.
Key words: botanical nematicide, Inula viscosa, management, Meloidogyne javanica, nematode, phytochemical, root-knot nematode,
The root-knot nematode Meloidogyne javanica causes
serious damage in vegetable crops in Israel, especially
in organic vegetable production systems. Incorporation
of organic amendments into the soil or soil solarization
does not always produce sufficient nematode control.
While the use of resistant cultivars or rootstocks is an
effective nematode management tool, they are not
available in all vegetable crops. Further, nematode re-
sistance, such as that in tomato, is often undermined by
high soil temperatures such as those that prevail in Is-
rael. Consequently, nematode management strategies
that can be used in organic farming systems are in de-
mand and one such practice may be use of natural
“nematicides.” Such products also may be used in con-
ventional farming systems due to concerns for environ-
mental and food safety.
Chemicals produced by plants are a potential source
of new chemistry for development of new pesticidal
compounds. Nematicidal phytochemicals are generally
safe for the environment and humans (Chitwood,
2002). Chinese herbal remedies may be a source of new
nematicidal compounds (Ferris and Zheng, 1999;
Zasada et al., 2002). Many nematicidal phytochemicals
from a great variety of chemical structures have been
isolated from numerous plant families (Gommers and
Bakker, 1988; Chitwood, 2002). A majority of these ne-
maticidal phytochemicals isolated have been from the
plant family Asteraceae (Gommers and Bakker, 1988).
?-Terthienyl and related compounds were isolated
from Tagetes spp. and have been shown to be nemati-
cidal at low concentrations in vitro (Uhlenbroek and
Bijloo, 1958, 1959). These phytochemicals, however,
were not effective in nematode control in soil (Gom-
mers and Bakker, 1988).
Polyacetylenes are another chemical group from the
Asteraceae with nematicidal activity. For example, ne-
maticidal polyacetylenes have been isolated from flow-
ers of Carthamus tinctorius and roots of Cirsium japonicum
(Kogiso et al., 1976; Kawazu et al., 1980), and dithio-
acetylenes have been isolated from Milleria quinqueflora,
Iva xanthiifolia, Ambrosia artemisiifolia, Ambrosia trifida,
Schkuhria pinnata, and Eriophyllym caespitosum (Gom-
mers and voor in ’t Holt, 1976). Thiarubrine C isolated
from the roots of Rudbeckia hirta has been shown to
have nematicidal activity against M. incognita and Prat-
ylenchus penetrans (Sánchez de Viala et al., 1998).
Unfortunately, none of these compounds or their
derivatives has been developed into commercial nema-
ticides. Plant essential oils, mainly monoterpenes, have
been evaluated for their nematicidal activity, and some
were highly effective in nematode suppression (Oka et
al., 2000; Oka, 2001). However, use of natural essential
oils as nematicides is not cost effective. Various neem
tree (Azadirachta indica A. Juss.) preparations are well
known, commercially available nematode control prod-
ucts derived from plants (Mojumdar, 1995).
Recently, elecampane (Inula viscosa, syn. Cupularia
viscosa, Dittrichia viscosa) (Asteraceae), a widespread
plant in Mediterranean countries, has been found to
have nematicidal activity in the shoot (Oka et al., 2001).
This plant has antifungal activity as well, and several
foliar fungal diseases have been controlled by the plant
extracts (Cohen, 1998; Wang et al., 2004). Another spe-
cies, I. helenium, has been known to have anthelmintic
activity, probably due to sesquiterpenoid lactones such
as alantolactone (Mahajan et al., 1986; Bourrel et al.,
1993). Sesquiterpenic acids (costic acid and isocostic
acid) from I. viscosa leaf extracts were found to be the
nematicidal phytochemicals (Oka et al., 2001). A mix-
ture of these compounds was toxic to M. javanica at
concentrations as low as 50 mg/kg in soil. However,
formulating the plant extract is essential for commer-
cial use of the nematicidal extracts. In the present
study, the toxicity of formulated plant extracts of I. vis-
cosa against M. javanica was evaluated in laboratory,
growth chamber, microplot, and field experiments.
Received for publication 10 January 2005.
1Nematology Unit, Gilat Research Center, Agricultural Research Organiza-
tion, M. P. Negev 85280, Israel.
2Agrogene Ltd., Kibbutz Kramim 84963, Israel.
3Faculty of Life Sciences, Bar-Ilan University, Ramat-Gan 52900, Israel.
The authors thank N. Tkachi and S. Shuker for their technical assistance.
This paper was edited by J. A. LaMondia.
Journal of Nematology 38(1):46–51. 2006.
© The Society of Nematologists 2006.
In conclusion, these results suggest that the EC for-
mulations of I. viscosa extract are potential nematicides
that can be used in organic and conventional agricul-
tural systems if the formulations are improved for soil
drenching or chemigation. A disadvantage of this for-
mulation and the active ingredient is the phytotocixity
that does not allow use of the product during the grow-
ing season. Non-phytotoxic nematicidal compounds
from plants must be found and developed into a com-
Bourrel, C., Vilarem, G., and Perineau, F. 1993. Chemical analysis,
bacteriostatic and fungistatic properties of the essential oil of Elecam-
pane (Inula helenium L.). Journal of Essential Oil Research 5:411–417.
Chitwood, D. J. 2002. Phytochemical-based strategies for nematode
control. Annual Review of Phytopathology 40:221–249.
Cohen, Y. 1998. Preparation and use of Inula extracts as a fungicide
for the control of plant diseases. United States Patent No. 5,837,253.
Ferris, H., and Zheng, L. 1999. Plant sources of Chinese herbal
remedies: Effects on Pratylenchus vulnus and Meloidogyne javanica.
Journal of Nematology 31:241–263.
Gommers, F. J., and Bakker, J. 1988. Physiological diseases induced
by plant responses or products. Pp. 3–22. in G. O. Poinar Jr. and H.-B.
Jansson, eds. Diseases of nematodes, vol. 1. Boca Raton, FL: CRC
Gommers, F. J., and voor in ’t Holt, D. J. M. 1976. Chemotaxonomy
of Compositae related to their host suitability for Pratylenchus pen-
etrans. Netherlands Journal of Plant Pathology 82:1–8.
Hussey, R. S., and Barker, K. R. 1973. A comparison of methods of
collecting inocula of Meloidogyne spp., including a new technique.
Plant Disease Reporter 57:1025–1028.
Kawazu, K., Nishii, Y., and Nakajima, S. 1980. Two nematicidal
substances from roots of Cirsium japonicum. Agricultural and Biologi-
cal Chemistry 44:903–906.
Kogiso, S., Wada, K., and Munakata, K. 1976. Isolation of nemati-
cidal polyacetylenes from Carthamus tinctoris L. Agricultural and Bio-
logical Chemistry 40:2085–2089.
Mahajan, R., Singh, P., Bajaj, K. L., and Kalsi, P. S. 1986. Nemati-
cidal activity of some sesquiterpenoids against root-knot nematode
(Meloidogyne incognita). Nematologica 32:119–123.
Mojumdar, V. 1995. Effects on nematodes. Pp. 129–150 in H.
Schmutterer, ed. The neem tree, Azadirachta indica A. Juss., and other
meliaceous plants: Source of unique natural products for integrated
pest management, industry, and other purposes. Weinheim, Ger-
Oka, Y. 2001. Nematicidal activity of essential oil components
against the root-knot nematode Meloidogyne javanica. Nematology 3:
Oka, Y., and Ben-Daniel, B. H. 1999. Nematicidal preparations
from Inula. Israel Patent No. 132543.
Oka, Y., Ben-Daniel, B. H., and Cohen, Y. 2001. Nematicidal activity
of powder and extracts of Inula viscosa. Nematology 3:735–742.
Oka, Y., Ben-Daniel, B. H., and Cohen, Y. 2003. Nematicidal and
fungicidal activity in soil of formulations of Inula viscosa (L.) Aiton.,
vol. II. Pp. 275 in 8th International Congress of Plant Pathology, 2–7
February, Christchurch, New Zealand.
Oka, Y., Nacar, S., Putievsky, E., Ravid, U., Yaniv, Z., and Spiegel, Y.
2000. Nematicidal activity of essential oils and their components
against the root-knot nematode. Phytopathology 90:710–715.
Öksüz, S., and Topçu, G. 1991. A eudesmanolide and other con-
stituents from Inula graveolens. Phytochemistry 31:195–197.
Sánchez de Viala, S., Brodie, B. B., Rodriguéz, E., and Gibson, D.
M. 1998. The potential of thiarubrine C as a nematicidal agent
against plant-parasitic nematodes. Journal of Nematology 30:192–
Shtacher, G., and Kashman, Y. 1970. 12-Carboxyeudesma-3,11(13)-
diene. A novel sesquiterpenic acid with a narrow antifungal spectrum.
Journal of Medicinal Chemistry 13:1221–1223.
Uhlenbroek, J. H., and Bijloo, J. D. 1958. Investigations on nema-
ticides. I. Isolation and structure of a nematicidal principle occurring
in Tagetes roots. Recueil des Travaux Chimiques des Pays-Bas 77:
Uhlenbroek, J. H., and Bijloo, J. D. 1959. Investigations on nema-
ticides. II. Structure of a second nematicidal principle isolated from
Tagetes roots. Recueil des Travaux Chimiques des Pays-Bas 78:382–
Ulubelen, A., Öksüz, S., and Gören, N. 1987. Sesquiterpene acids
from Inula viscosa. Phytochemistry 26:1223–1224.
Wang, W. Q., Ben-Daniel, B. H., and Cohen, Y. 2004. Control of
plant diseases by extracts of Inula viscosa. Phytopathology 94:1042–
Zasada, I. A., Ferris, H., and Zheng, L. 2002. Plant source of Chi-
nese herbal remedies: Laboratory efficacy, suppression of Meloidogyne
javanica in soil, and phytotoxicity assays. Journal of Nematology 34:
Zdero, C., Bohlmann, F., Haegi, L., and King, R. M. 1988. Eudes-
manolides and other constituents from Cratystylis conocephala. Phyto-
Nematode Control with Inula viscosa Extracts: Oka et al. 51