Applied Soil Ecology 44 (2010) 101–115

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Applied Soil Ecology

journal homepage: www.elsevier.com/locate/apsoil

Review

Mechanisms of nematode suppression by organic soil amendments—A review

Y. Oka *
Nematology Unit, Gilat Research Center, M.P. Negev 85280, Israel

A R T I C L E I N F O A B S T R A C T

Article history: Application of organic soil amendments is a traditional control method for plant–parasitic nematodes
Received 29 June 2009 and it is considered a part of nematode-management programs. A variety of organic amendments, such
Received in revised form 8 November 2009 as animal and green manures, compost, nematicidal plants and proteinous wastes, are used for this
Accepted 13 November 2009
purpose, but nematode control efficacy is not always satisfactory. Elucidation of nematode-control
mechanisms in amended soil may lead to improved efficacy or the development of more effective control
Keywords: techniques, although the effects of organic amendments on nematodes, microbial communities, plants
Antagonist
and soil environments are very complex. Possible mechanisms involved in nematode suppression are:
Control
Nematicidal compound
(1) release of pre-existing nematicidal compounds in soil amendments, (2) generation of nematicidal
Organic amendment compounds, such as ammonia and fatty acids, during degradation, (3) enhancement and/or introduction
Plant–parasitic nematode of antagonistic microorganisms, (4) increase in plant tolerance and resistance, and (5) changes in soil
physiology that are unsuitable for nematode behavior. Combinations of these mechanisms, rather than a
single one, appear to produce nematode suppression in amended soils.
ß 2009 Elsevier B.V. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 101
2. Release of pre-existing nematicidal phytochemicals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 102
2.1. Neem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 102
2.2. Asteraceae plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 102
2.3. Other plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 103
3. Generation of nematicidal compounds during degradation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 103
3.1. Glucosinolate-derivative compounds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 103
3.2. Organic acids. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 104
3.3. Nitrogenous compounds. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 105
3.4. Glycoside-derivative compounds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 106
3.5. Other compounds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 106
4. Enhancement of antagonistic organisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 106
4.1. Plant residues . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 107
4.2. Animal manure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 108
4.3. Chitinous materials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 108
4.4. Compost . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 108
4.5. Other materials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 109
5. Increase in plant tolerance/resistance. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 109
5.1. By microorganisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 109
5.2. By natural compounds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 110
6. Physical changes in the soil. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 110
7. Outlook. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 111
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 111

1. Introduction

* Tel.: +972 8 9928659; fax: +972 8 9926485. Plant–parasitic nematodes in intensive crop-production sys-
E-mail address: okayuji@volcani.agri.gov.il. tems have been controlled mainly by chemical soil fumigants and

0929-1393/$ – see front matter ß 2009 Elsevier B.V. All rights reserved.
doi:10.1016/j.apsoil.2009.11.003
102 Y. Oka / Applied Soil Ecology 44 (2010) 101–115
nematicides for decades. However, several fumigants and nema-
ticides have been withdrawn from the market in the last few
decades due to concerns about the environment and human health
(Rich et al., 2004). Moreover, consumer demand for safe food has
forced farmers to reduce the use of chemical pesticides. The phase-
out of methyl bromide in 2005 in most of the world’s developed
countries severely affected nematode-control strategies. Cur-
rently, only a small number of nematicides, which are organopho-
sphates and carbamates, and soil fumigants are available for
nematode control in most countries. Among pesticides, nemati-
cides are the most problematic because these chemicals are highly
toxic to humans, applied to the soil and therefore likely to
contaminate the groundwater, and some of them are also absorbed
by plants.
Use of organic soil amendments is a traditional cultural practice
to improve soil fertility and structure; it is also known as a control
method for soilborne diseases, including plant–parasitic nema-
todes. Organic amendments can also be applied in organic or
sustainable farming systems, and enable conventional farmers to
reduce their use of nematicide. Many types of organic amendments
have been tested for nematode control, and these are reviewed in
Rodrı́guez-Kábana (1986). The most common amendments are
wastes or byproducts of agricultural industries, such as animal
manures, compost and plant residues. One of the problems with
using this control method for nematodes is inconsistent control
efficiency, which is highly influenced by amendment and soil type.
Understanding the mechanisms involved in nematode suppression
in amended soils is essential to improving this method and
obtaining maximum control efficacy. This review focuses on the
possible mechanisms governing nematode suppression in
amended soils, rather than on amendment types per se, and
discusses possibilities for increasing nematode control efficacy by
amendments.
2. Release of pre-existing nematicidal phytochemicals
Plants have served as pesticides since ancient times. Natural
and synthetic analogs based on natural compounds in plants
have been developed for use in pest control, e.g. the use of
pyrethrin and pyrethroids as insecticides. Many nematicidal
compounds have been isolated and identified from plants
(Gommers and Bakker, 1988; Chitwood, 2002). However, only
a small number of plants known to contain such compounds have
been used as soil amendments for nematode control in
commercial fields. Although many plants have been used as soil
amendments to control nematodes in small-scale experiments,
only a few reports have identified the nematicidal compound(s)
in such plants. Unfortunately, to the best of my knowledge,
concentrations of pre-existing ‘‘active’’ nematicidal compounds
released from plant preparations in amended soils, which could
indicate a direct effect of nematicidal compounds on nematodes,
have never been measured.
2.1. Neem
Neem (Azadirachta indica) is known as a ‘‘miracle’’ tree due
mainly to its medicinal and pesticidal properties. The main use of
this plant in pest control involves its seed oil as an insecticide.
Limonoids are thought to be the main constituents responsible for
neem’s insecticidal activity, and azadirachtin is the most important
of these. Many neem preparations, including leaves, oil cakes and
kernel oils, have been tested for their nematicidal activity
(Mojumdar, 1995; Akhtar, 2000), and the insecticidal limonoids
from kernel oils, including azadirachtin, nimbin and salannin, have
been reported to be the main nematicidal compounds as well
(Devakumar et al., 1985; Akhtar, 2000). Insecticidal preparations
(seed kernel extracts) could be used for nematode control, but
large volumes of such extracts are required for this purpose, and
they are generally not cost-effective. A neem extract containing
10% azadirachtin was nematicidal to Meloidogyne javanica
juveniles in alkaline sandy soil (pH 8.5) at concentrations higher
than 0.05 g kg 1, or at higher than 0.17 g kg 1 for its formulation
(Oka et al., 2007c). Application rates of over 500 L ha 1 of such
formulated neem extracts could be required for nematode control.
The most commonly used neem preparation for soil applications is
oil cakes, which are the seed residues following oil extraction.
Neem oil cakes serve as fertilizer, and several studies have reported
their suppression of nematodes (Akhtar and Mahmood, 1996;
Akhtar, 1998; Abbasi et al., 2005). However, a direct effect of
nematicidal compounds in the oil cakes (i.e. limonoids), which may
be present in low concentrations after oil extraction, on nematodes
has not been shown. Since the oil cakes are rich in nutrients, other
nematicidal compounds, such as ammonia, which may be
generated during the oil cake’s degradation, could be involved
(Abbasi et al., 2005).
2.2. Asteraceae plants
Many nematicidal compounds have been isolated from
Asteraceae plants. The most studied of these are the polythienyls,
especially a-terthienyl from Tagetes spp. and other Asteraceae
(Gommers and Bakker, 1988). The nematicidal mode of action of a-
terthienyl has been intensively investigated, and involvement of
singlet oxygen upon irradiation has been suggested. However,
polythienyls and their synthetic analogs had almost no nemati-
cidal activity in the soil (Gommers and Bakker, 1988). Because
nematodes are likely to be killed inside the roots rather than by
secretion of nematicidal compounds in the rhizosphere (Topp et
al., 1998), Tagetes spp. are usually used as a rotation crop for
nematode control, mainly for Pratylenchus and Meloidogyne spp.
However, incorporation of Tagetes plants is also effective. Foliage of
Tagetes patula incorporated into soil infested with Meloidogyne
incognita reduced nematode infection, but the reduction was not
specific to amendment with Tagetes (Ploeg, 2000). Non-volatile
nematicidal compounds (myristic and dodecanoic acids) and
essential oils were isolated from flowers of Tagetes erecta
(Debprasad et al., 2000), and aqueous extracts of the plant
reduced the galling index of tomato roots caused by M. incognita
(Natarajan et al., 2006). Such nematicidal compounds may be
involved in nematode suppression in soil amended with the foliage
of Tagetes plants.
Use of other Asteraceae plants as soil amendments for
nematode control has been reported in a few studies. A plant
preparation of Artemisia dracunculus at 2–4% in soil reduced
Ditylenchus dipsaci, probably due to flavonoid compounds (Tim-
chenko and Maiko, 1989). Extracts of other Artemisia spp., A.
verlotorum and A. absinthium, showed nematicidal activity against
M. incognita (Dias et al., 2000). Foliage of wild chrysanthemum
(Chrysanthemum coronarium) showed nematicidal activity against
M. javanica when it was incorporated into the soil, and nematode
juveniles were killed by exposure to aqueous plant extracts in vitro
(Bar-Eyal et al., 2006). In another study, soil amendment with
flowers, leaves, roots or seeds of C. coronarium, and flowers from
several other species of Asteraceae (Chrysanthemum segetum,
Calendula maritima, Calendula officinalis and Calendula suffruticosa)
at 10 g L 1 soil significantly reduced reproduction rates of
Meloidogyne artiellia in pot trials (Pérez et al., 2003). Essential
oil of C. coronarium at concentrations of 20–80 ml L 1 soil also
significantly reduced the nematode’s reproduction rate. Tissue
extracts of Gaillardia pulchella were lethal to various plant–
parasitic nematodes, and amendment of soils with roots, stems or
leaves of G. pulchella was effective in controlling M. incognita (Tsay
 Y. Oka / Applied Soil Ecology 44 (2010) 101–115
et al., 2004). None of these studies, however, suggested active
nematicidal compounds in the plants. Leaf powder of Inula viscosa,
which grows widely in the Mediterranean basin, reduced galling
index of tomato and cucumber plants in pot experiments with
alkaline sandy soil (Oka et al., 2001). Sesquiterpenic acids were
suggested as the main nematicidal compounds in this plant.
Formulated leaf extracts of I. viscosa were tested in a field trial: only
slight control was obtained, although they had shown good control
efficacy in pot experiments (Oka et al., 2006a). The nematode-
suppressive effect of Rudbeckia hirta may be due to thiarubrine C, a
nematicidal polyacetylene which was isolated from the plant and
tested for nematicidal activity (Hijink and Suatmadji, 1967;
Sànchez de Viala et al., 1998). With the exception of Tagetes
spp., use of Asteraceae plants containing nematicidal compounds
as soil amendments in field experiments or in commercial fields for
nematode control is not a popular practice.
2.3. Other plants
Crotalaria spp. are used as a cover crop in crop rotations, and
occasionally incorporated into the soil, due to their nematode-
suppressive effect and nitrogen-fixing ability (Wang et al., 2002).
Although monocrotaline, which inhibited M. incognita movement,
was isolated from Crotalaria spectabilis (Fassuliotis and Skucas,
1969), the role of this compound in nematode suppression by the
plant residues in the soil is not clear. Non-host or poor host status
of the plant toward several important nematodes is expected to
play an important role in nematode suppression (Wang et al.,
2002). Two alcohols, which inhibited M. incognita hatching, were
isolated from velvet bean (Mucuna pruriens) (Nogueira et al.,
1996). This leguminous plant is generally used as a cover crop or
green manure to reduce some important nematode species
(Weaver et al., 1998; Ritzinger and McSorley, 1998). Some
leguminous plants are known to contain lectins, such as
concanavalin A from Canavalia ensiformis, which may disrupt
nematode behaviors, such as host-finding (Marban-Mendoza et
al., 1987). Co-cultivation of C. ensiformis with tomato reduced root
galling caused by M. incognita and Nacobbus aberrans (Marban-
Mendoza et al., 1989). Nevertheless, a direct effect of lectins or
other bioactive compounds in leguminous plant materials
incorporated in the soil on nematode suppression has not been
confirmed (Marban-Mendoza et al., 1989; Morris and Walker,
2002). Ricin is a highly toxic lectin from castor bean (Ricinus
communis), which was found to inhibit the mobility of M. incognita
at relatively high concentrations (EC50 for the effects on mobility:
33 mg L 1) (Rich et al., 1989). Castor bean is also a potential
rotation crop and green manure for suppression of Meloidogyne
arenaria (Rodrı́guez-Kábana et al., 1989; Ritzinger and McSorley,
1998), and its oil cake was nematicidal when incorporated in
the soil (Akhtar and Mahmood, 1996). Although it remains
unconfirmed, this nematicidal lectin may be involved in the
nematode suppression by castor bean oil cake (Lear, 1959; Akhtar
and Mahmood, 1996).
Many essential oils of medicinal plants and herbs have been
reported to be nematicidal (Oka et al., 2000; Park et al., 2005), but
the effect of their plant materials when incorporated into the soil
has not been well studied. Soil amendments with several oriental
herbal medicines at 0.2% (w/v) reduced M. incognita infection on
tomato (Kim et al., 2003). The most effective treatments were
root bark of Paeonia suffructicosa and stem bark of Cinnamomum
cassia; however, nematicidal compounds in the plant materials
have not been confirmed. Plants containing nematicidal essential
oils may be used as soil amendments, and the most practical
method may be planting them as a cover crop and incorporating
their foliage in the soil, preferably in conjunction with tarping with
plastic film.
103
Use of plants containing nematicidal compounds in crop
rotations and their incorporation into the soil may be more
effective in nematode control than cropping non-host plants
without nematicidal compounds (Halbrendt, 1996). However,
several factors, such as nematode-host status of the candidate
plants, timing of incorporation into the soil, phytotoxicity to crops
and stability of nematicidal compounds in the soil, should be
studied to obtain maximum control efficacy. Another important
factor for successful control using nematicidal plant preparations
is soil type. Nematode control by plant preparations containing
nematicidal compounds seems to be more effective in light soils,
such as sandy soils, than in heavy soils, because in the latter, active
compounds may be absorbed by the clay and inactivated.
3. Generation of nematicidal compounds during degradation
Many organic amendments which do not contain pre-existing
nematicidal phytochemicals release nematicidal compounds dur-
ing their degradation or decomposition in the soil. Such amend-
ments include several green and animal manures, and materials
with high nitrogen contents. Nematicidal compounds in this
category have been studied more thoroughly than other potential
mechanisms, likely due to their relatively easy detection in soil,
their effectiveness towards other soilborne pathogens, their simple
chemical structures and their availability from commercial
sources. In this section, glucosinolate-derivative compounds,
organic acids, nitrogenous compounds and others are discussed.
3.1. Glucosinolate-derivative compounds
Cultivation and incorporation of cover/rotation crops, espe-
cially Brassicaceae plants, occasionally suppresses soilborne
diseases, including nematodes. Utilization of volatile toxic
compounds, such as isothiocyanates generated from the glucosi-
nolates in such crops, for soilborne disease control is generally
termed biofumigation (Kirkegaard et al., 1993). Isothiocyanates
are known to possess broad pesticidal activity against weeds,
bacteria, fungi and nematodes (Matthiessen and Kirkegaard, 2006),
and are similar or relative to compounds found in commercial soil
fumigants, such as metham sodium and dazomet, which release
methyl isothiocyanate into the soil. Nematode suppression by
biofumigation with Brassicaceae plants has been attempted in
several regions worldwide, mainly with rapeseed (Brassica napus)
and Indian mustard (Brassica juncea) (Mojtahedi et al., 1991, 1993;
Walker and Morey, 1999; Ploeg and Stapleton, 2001; Stirling and
Stirling, 2003; Zasada and Ferris, 2004; Rahman and Somer, 2005).
The efficacies for soilborne disease control were generally variable
and inconsistent, a trend which seemed more salient with
nematodes than with soilborne fungi (Matthiessen and Kirkegaard,
2006). In-vitro assays revealed that isothiocyanates from Brassi-
caceae plants were nematicidal to juveniles of M. incognita and
Tylenchulus semipenetrans at concentrations as low as 10 mM
(Zasada and Ferris, 2003; Lazzeri et al., 2004a). However, several
studies have shown that nematode control efficacy and nematode
reproduction in treated soils are not correlated with glucosinolate
contents in plants (Potter et al., 1998; McLeod and Steele, 1999).
Although glucosinolates are thought to play an important role in
nematode suppression, non-glucosinolate compounds, such as
other sulfur-containing compounds (Bending and Lincoln, 1999),
as well as biological and physiological factors, may also be involved
(Mazzola et al., 2001). Although the effects of soil type on
biofumigation efficacy have not been well studied, sandier soils
with low organic matter content appear to allow better
performance of the biofumigant.
Before selecting a plant for biofumigation purposes, the host
range of the target nematode(s) needs to be checked, because most
104 Y. Oka / Applied Soil Ecology 44 (2010) 101–115
Brassicaceae used as cover crops are hosts of some important
nematodes, such as Meloidogyne spp. (McLeod and Steele, 1999;
McLeod et al., 2001), and host Brassicaceae plants may increase
nematode populations instead of reducing them. Biofumigant
plants that are non-hosts or poor hosts, or are nematode-resistant,
are strongly preferred. A study in Australia showed that M. javanica
reproduced on B. juncea and B. napus at rates which increased the
nematode population in the soil during their growth period in hot
seasons; however, nematode proliferation could be prevented if
these plants were grown in the winter under low temperatures
(Stirling and Stirling, 2003). Use of dried pellets of glucosinolate-
containing plants can solve the problem of nematode population
buildup in the field, while adding a biofumigation effect (Lazzeri et
al., 2004b). Again, to obtain maximum control efficacy from
biofumigation, several factors must be considered in addition to
host status for nematodes, including: the optimum plant growth
stage for soil incorporation (probably when the glucosinolate
content reaches maximum levels), biomass of the plant, and
adequate soil moisture for plant degradation and gas diffusion into
the soil while preventing rapid gas escape from the soil to the
atmosphere. Variations in glucosinolate profiles and concentra-
tions exist among Brassicaceae crops and their developmental
stages (Bellostas et al., 2007).
An effective way of enhancing the nematode-control efficacy of
biofumigation in small areas is to combine the incorporation of
Brassicaceae plants with soil tarping using plastic film, which may
prevent rapid emission of volatile nematicidal compounds from
the soil to the atmosphere, and increase the soil temperature via a
soil-solarization effect if performed in hot seasons. Elevation in soil
temperatures due to soil solarization has been shown to improve
the control efficacy of amendments with Brassicaceae crops
(Gamliel and Stapleton, 1993; Stapleton and Duncan, 1998; Ploeg
and Stapleton, 2001). Combinations of sublethal soil temperatures
(30–38 8C) and the biofumigation effect (toxic volatile com-
pounds) may have a synergistic effect on nematode-control
efficacy. Sublethal temperatures may render nematodes more
sensitive to toxic compounds or to antagonistic microorganisms.
Because nematode control has been obtained by soil solarization
plus biofumigation with non-Brassicaceae plants, such as pepper
plant residues (Piedra Buena et al., 2007), this method does not
appear to be specific to glucosinolate-containing plants. Other
studies on the effects of fresh organic amendments and soil tarping
on fungal pathogens have suggested that toxic compounds,
elevated temperature, anaerobic and reducing soil conditions,
and biological activity are involved in the control (Gamliel and
Stapleton, 1993; Blok et al., 2000).
Nitriles are another group of toxic compounds derived from
glucosinolates. Simple nitriles have been shown to be involved in
direct and indirect plant defense responses upon attack of Pieris
rapae (Lepidoptera) (Mumm et al., 2008). The role of nitriles in
nematode suppression is not clear.
3.2. Organic acids
Nematodes are often suppressed in flooded fields. In addition to
depletion of oxygen, several compounds, which are toxic to
nematodes, are thought to be generated under flood conditions.
The best-studied nematicidal compounds generated by the
decomposition of amendments in saturated soil are the short-
chain fatty acids, including acetic, butyric, formic and propionic
acids (Johnston, 1959; Patrick et al., 1965; Sayre et al., 1965). These
organic acids are generally produced by fermentation of carbon-
rich organic matter by microorganisms under anaerobic condi-
tions. A population of Tylenchorhynchus martini was reduced by the
short-chain fatty acids generated by the microbial activity of the
anaerobic bacterium Clostridium butyricum (Johnston, 1959). These
and other organic acids have also been identified in decomposing
organic matter, such as rye (Secale cereale), timothy (Phleum
pretense), rice bran, glucose and unsulfured molasses, and found to
be toxic to plant–parasitic nematodes (Patrick et al., 1965; Sayre
et al., 1965; Taba et al., 2006) and other soilborne pathogens (Kubo
et al., 2005; Momma et al., 2006). In particular, butyric acid has
been tested as an alternative to synthetic soil fumigants for control
of nematodes and fungal pathogens (Browning et al., 2004, 2006;
McElderry et al., 2005). Butyric acid at concentrations as low as
8.8 mg kg 1 soil resulted in 100% mortality of Tylenchorhynchus
spp. over the course of 7 days (McElderry et al., 2005), while higher
concentrations of the acid (0.88–8.8 g kg 1 soil) in the soil reduced
a Pratylenchus penetrans population by 98–100% and root galls of
Meloidogyne hapla and M. incognita by 73–100% (Browning et al.,
2006). In another study, a 2-day incubation in sand amended with
butyric acid at 0.88 g kg 1 reduced populations of the plant–
parasitic nematodes Hoplolaimus galeatus, Longidorus sylphus,
Tylenchorhynchus claytoni and Helicotylenchus robustus, whereas
bacterivorous nematodes were unaffected (Browning et al., 2004).
However, a study showed that concentrations of formic and acetic
acids detected in rye-amended soil were not correlated with
suppression of M. incognita (McBride et al., 2000). Other chemical,
physical or biological factors were suggested to be involved in the
nematode suppression. A role in nematode suppression was
suggested for nematicidal hydroxamic acids in rye residues
(Zasada et al., 2005).
Organic acids are very toxic to plant–parasitic nematodes in
vitro (Taba et al., 2006), although the nematicidal activity of
organic amendments that release organic acids during decom-
position in soil is highly influenced by soil conditions, including
oxygen concentrations, redox potential, pH, microbial activity and
soil temperature. Generally, higher nematicidal or fungicidal
activity is obtained when soil amended with carbon-rich materials
is kept under anaerobic conditions, either by flooding and/or soil
tarping with plastic film (Gamliel and Stapleton, 1993; Browning
et al., 1999; Blok et al., 2000; Momma et al., 2006). Under such
conditions, oxygen is depleted mainly by bacterial activity, and
redox potential and soil pH are decreased by the organic acids
generated from the amendments (Browning et al., 1999; Blok et al.,
2000; Momma et al., 2006). Several factors in this method, termed
reductive soil disinfestation, can be manipulated to increase the
control efficacy. A more rapid decrease in soil redox potential may
be achieved by elevating the soil temperature, which in turn
increases the microbial activity in the soil (Blok et al., 2000). Only
non-ionized forms of the organic acids can cross the nematodes’
cell membrane and affect them: lowering the soil pH increases the
percentage of non-ionized organic acids, thereby enhancing
nematicidal activity, in addition to the direct adverse effect of
low pH on nematodes (McElderry et al., 2005). The pKa of acetic,
butyric and propionic acids is about 4.8, and a soil pH that is lower
than this value may greatly enhance nematicidal activity (Banage
and Visser, 1965). Theoretically, almost all of these acids are in
non-ionized forms at a soil pH of 2.0. Such a low soil pH, in turn,
reduces the activity of microorganisms, particularly bacteria,
which can oxidize the organic acids, and therefore the stability of
the organic acids in the soil is increased (McElderry et al., 2005).
For these reasons, reductive soil disinfestation is more effective in
acid than in alkaline soils. Addition of acidifiers to the soil or
amendments could potentially enhance the nematicidal activity of
organic acids. The organic acids are also phytotoxic (Lynch, 1978),
and planting should therefore be done after their decomposition
and recovery of the soil to its original pH. Nevertheless, it should be
remembered that high nematicidal or fungicidal activity in
reductive soil disinfestation is suggested to result from the
synergistic or additive effects of anaerobic conditions, low soil
pH, elevated soil temperature, toxic compounds and soil microbial
 Y. Oka / Applied Soil Ecology 44 (2010) 101–115
activities (Browning et al., 1999; Momma et al., 2006). Reductive
soil disinfestation may adversely affect soil health by, for example,
increasing the concentrations of soil elements to toxic levels via
low pH and lowered oxygen concentrations in the soil. However,
such adverse effects are temporary and the original soil conditions
are generally restored before planting. In fact, reductive soil
disinfestation using wheat bran as an amendment and plastic sheet
for soil tarping followed by flooding is commonly used in Japan for
some vegetable crops (Momma et al., 2006).
Another source of short-chain fatty acids from organic
amendments is animal manures. Acetic, propionic, butyric,
isovaleric and caproic acids, which were responsible for the death
of Verticillium dahliae microsclerotia, were generated when liquid
hog manure was acidified or added to acid soil (Tenuta et al., 2002;
Conn et al., 2005). Anaerobically digested slurry and liquid swine
manure had suppressive effects on Pratylenchus penetrans and
Heterodera glycines, respectively, and involvement of volatile fatty
acids was suggested (Min et al., 2007; Xiao et al., 2007). Among the
fatty acids, valeric acid was the most toxic to P. penetrans, while
isobutyric acid was the least toxic, and the effect of each fatty acid
on the nematode was considered additive rather than synergistic
(Mahran et al., 2008b). To obtain higher control efficacy by fatty
acids, animal manures and soil conditions can be manipulated, i.e.
by lowering the pH of the animal manures or soil (Mahran et al.,
2008a), and fermenting the manures before application. The
effectiveness of liquid hog manure was improved by acidification
of slightly acidic soils with sulfuric acid when concentrations of
volatile fatty acids in the manure were low (Mahran et al., 2008a).
3.3. Nitrogenous compounds
A negative linear relationship was found between nitrogen
content in organic amendments applied to soil and infestation of
plants by root-knot nematodes (Rodrı́guez-Kábana et al., 1987). A
positive relationship was found between the carbon-to-nitrogen
(C/N) ratio in the amendments and nematode infestation of plants
(Rodrı́guez-Kábana et al., 1987). Nitrogenous compounds, mainly
ammonia (NH3), are generated from organic materials with low C/
N ratios in the soil. The most popular and practical of these
amendments is animal manure (Kaplan and Noe, 1993; Lazarovits
et al., 2000; Riegel and Noe, 2000; Oka et al., 2007a). Other organic
materials with high nitrogen contents include oil cakes, cottonseed
meal, crab shells, feather meal, bone meal, blood meal, horn meal
and fungal mycelium, among others (Walker, 1971; Rodrı́guez-
Kábana, 1986; Stirling, 1991). Ammonia is generated from organic
materials being decomposed by soil microorganisms, and is known
to play an important role in the suppression of plant–parasitic
nematodes and fungi for a relatively short time (a few days to
weeks, depending on the soil environment) after application
(Rodrı́guez-Kábana, 1986; Rodrı́guez-Kábana et al., 1987; Spiegel
et al., 1987; Oka et al., 1993; Lazarovits et al., 2000; Tenuta and
Lazarovits, 2002). The biocidal mode of action of ammonia is not
clear, but several mechanisms are thought to be involved: cell
membrane disruption (Rush and Lyda, 1982), elimination of proton
gradients across membranes (Docherty and Snider, 1991) and
exhaustion of the chemical energy of cells removing cytosolic
ammonia against a concentration gradient (Britto et al., 2001).
Ammonium (NH4+), the ionized form of ammonia, cannot cross the
cell membrane, and is not nematicidal (Oka et al., 1993). The
potential effectiveness of ammonia, in either anhydrous or
aqueous form, in nematode control has been demonstrated
(Rodrı́guez-Kábana et al., 1981; Oka and Pivonia, 2002), but the
use of these forms of ammonia has not been accepted commer-
cially for control of nematodes or fungi. A limitation to the use of
ammonia-releasing organic amendments for nematode control is
that the large amounts required for satisfactory control are often
105
phytotoxic, or simply not cost-effective (Rodrı́guez-Kábana et al.,
1987; Stirling, 1991).The nematicidal efficacy of NH4OH on tomato
plants in a sandy alkaline soil at doses of 1,000 and 2,000 kg
NH4OH-N ha 1 was equivalent to that of chemical soil fumigants
(Oka and Pivonia, 2002). Urea, which is converted to ammonia by
microbial ureases in the soil, showed good nematicidal activity
when it was applied at >300 mg N kg 1 soil (Rodrı́guez-Kábana
and King, 1980). When nematicidal concentrations of ammonia
were calculated based on ammonium concentrations and soil or
solution pH, exposure of M. javanica juveniles to 40 to 70 mg NH3-
N kg 1 soil for 7 days greatly reduced the number of juveniles
recovered from the soil (Oka et al., 2006b), and exposure of the
juveniles to ammonia at 9.3 mg L 1 for 40 h was lethal to 95% of the
nematode population (Oka et al., 1993). Therefore, manipulation
of soil environments may be needed to enhance the nematicidal
activity of ammonia-releasing amendments, and/or to reduce the
amount required for practical control.
The application rates of nitrogenous amendments required for
efficient nematode control are highly dependent on soil pH, since
the equilibrium of ammonia in the liquid phase of the soil with the
non-nematicidal ammonium is pH-dependent, as formulated by
the Henderson–Hasselbalch equation (Duplessis and Kroontje,
1964). In soil with pH 9.3, which is the pKa of ammonia at 24 8C,
only 50% of the generated ammonia remains as ammonia in the
soil, and the other half converts to non-nematicidal ammonium; if
the soil pH is raised to about 11, the ammonia becomes dominant,
and reaches nearly 100% of the total amount generated. Thus,
temporarily increasing soil pH is one potential way of enhancing
the control efficacy of ammonia-releasing amendments. The
nematicidal activity of broiler litter against M. javanica was
enhanced by transiently increasing the soil pH via the use of
alkaline amendments, such as cement kiln dust or alkaline-
stabilized biosolids (Oka et al., 2006b,c). On an organic farm,
application of slaked lime in combination with broiler litter
slightly but significantly reduced the root-galling index of pepper
plants caused by M. incognita (Oka et al., 2007a). This technique is
suitable for neutral to alkaline soils with low buffering capacities,
whose pH can be relatively easily increased. The increase in soil pH
is transient, returning to its original level after several weeks.
Another limiting factor for the use of ammonia-releasing
amendments is the instability of ammonia in the soil. Ammonia
is readily oxidized to nitrite (NO2 ), and then to nitrate (NO3 ) by
soil microorganisms, in a process called nitrification. Generally, soil
pH increases during the decomposition of amendments due to the
released ammonia, but the pH drops shortly thereafter, when
ammonia is oxidized to nitrite and nitrate. Unfortunately, nitrifica-
tion is faster in alkaline than in acid soils. If the ammonia
concentration can be maintained for longer periods in the soil,
nematode control efficacy should increase. Application of a chemical
nitrification inhibitor (nitrapyrin) in combination with organic or
chemical ammonia-releasing amendments was shown to increase
the nematicidal activity of the amendments against M. javanica (Oka
and Pivonia, 2003). Organic nitrification inhibitors can be used for
this purpose in organic farming systems, where synthetic chemicals
are not allowed. Some medicinal and herbal plants have been
reported to have nitrification-inhibiting activity; in particular,
karanja (Pongamia pinnata) and neem (A. indica) extracts were
found to be relatively effective at inhibiting nitrification (Sahrawat
and Mukerjee, 1977; Gnanavelrajah and Kumaragamae, 1999). The
nematicidal activities of chicken litter and chitin, alone or in
combination with neem extracts, were tested against M. javanica.
Soil application of these organic amendments or the neem extracts
alone reduced the root-galling index of tomato plants only slightly, if
at all, but application of the amendments in combination with the
neem extracts reduced root galling significantly (Oka et al., 2007c).
Soil analysis indicated that the neem extract inhibited nitrification of
106 Y. Oka / Applied Soil Ecology 44 (2010) 101–115
the ammonia released from the amendments and extended the
persistence of ammonia concentrations in the soil. Another
technique to enhance the nematicidal activity of organic amend-
ments is to combine amendment application with soil tarping. This
technique increases nematode control efficacy of nitrogenous
amendments via several mechanisms: the plastic sheet may
physically retain the ammonia in the soil for longer periods, induce
oxygen depletion, and increase soil temperature. Increased tem-
perature affects several factors: direct killing of the nematodes or
sublethal effects, increase in the vapor pressure of ammonia, which
allows the ammonia to diffuse deeper into the soil. High soil
temperatures (>30 8C) also reduce the activity of nitrifying bacteria,
and nitrification rate (Fdz-Polanco et al., 1994), and decrease the pKa
of ammonia (9.3 at 24 8C and 8.5 at 50 8C), which in turn theoretically
increases ammonia concentrations in the soil. (Gamliel and
Stapleton, 1993; Blok et al., 2000; Lazarovits et al., 2000; Momma
et al., 2006; Oka et al., 2007a).
Application of organic amendments with low C/N ratios is also
effective in acidic soils for the control of soilborne diseases and
nematodes. However, the suppression is achieved more slowly
than in neutral to alkaline soils. The compounds involved in acid
soils are several of the aforementioned fatty acids and a
nitrogenous acid. As already noted, the ammonia released from
amendments is oxidized to nitrite in the first stage of nitrification,
mainly by Nitrosomonas bacteria. In acidic environments, the
nitrification process is not as rapid as in alkaline environments, and
nitrite occasionally accumulates in the soil. Nitrite in the soil water
phase is in equilibrium with nitrous acid [HNO2], the non-ionized
form of nitrite, and nitrous acid is known to be highly toxic to fungi
and nematodes (Tsao and Oster, 1981; Oka et al., 1993; Lazarovits
et al., 2000; Tenuta and Lazarovits, 2002). Exposure of M. javanica
to nitrous acid at 4.6 mg L 1 caused 100% loss of infectivity (Oka
et al., 1993), and it was 300–500 times more effective at killing V.
dahliae microsclerotia than ammonia (Tenuta and Lazarovits,
2002). In contrast to ammonia, nitrous acid is dominant at low pH
due to its low pKa (3.33 at 24 8C), and is effective in acid soils.
Nitrous acid played an important role in the suppression of V.
dahliae and P. penetrans by liquid swine and hog manures in
slightly acidic soils, in addition to the nematicidal effect of the
released short-chain fatty acids (Conn et al., 2005; Mahran et al.,
2008a). Enhanced control activity may be achieved by lowering the
pH of the soil or manures with acids (Conn and Lazarovits, 2000).
3.4. Glycoside-derivative compounds
Several gramineous plants are known to suppress nematode
populations when they are incorporated into the soil as green
manures. Sudangrass and sorghum–sudangrass hybrids produced
a cyanogenic glycoside (dhurrin) which degraded into nematicidal
hydrogen cyanide, and controlled Meloidogyne hapla (Widmer and
Abawi, 2000, 2002). A correlation between reductions in root galls
caused by M. hapla and hydrogen cyanide contents was indicated
in sorghum–sudangrass hybrids (Widmer and Abawi, 2002). Other
cyanogenic plants, such as white clover (Trifolium repens) and flax
(Linum usitatissimum), were also effective at reducing root galls
(Widmer and Abawi, 2002). Another source of cyanogenic glyco-
side that can be used for nematode control is cassava (Manihot
esculenta) roots containing linamarin. The liquid by-product of
cassava root processing has been used for nematode control in
Brazil (Sena et al., 1982). The incorporation of rye cover crop before
planting eggplant kept population densities of M. incognita at
relatively low levels to mid growing season (McSorley and Dickson,
1995), and hydroxamic acids were suggested to play a role in
nematode control by rye incorporation (Zasada et al., 2005). In
intact rye, the cyclic hydroxamic acids occur as glycosides, which
are rapidly hydrolyzed by b-glucosidase and release hydroxamic
acids upon tissue disruption. High mortality of M. incognita
juveniles and mixed-stages of Xiphinema americanum was
obtained in in-vitro tests by exposure to some solutions of
hydroxamic acids at a concentration of 90 mg L 1. Concentrations
of such nematicidal compounds may serve as a potential indicator
in the selection of rye varieties for nematode control (Zasada et al.,
2007). Saponins are glycosides that occur widely in plants, and are
known to have antimicrobial activity (Sparg et al., 2004).
Commercial extracts of Quillaja saponaria, which is known to
contain saponins and polyphenols, have been used to control
nematodes in Chile (San Martin and Magunacelaya, 2005). Field
trials showed that application of a commercial formulation
containing the plant extract controlled nematodes, such as
Meloidogyne and Xiphinema spp., in vineyards and table grapes
as effectively as synthetic nematicides. Soil-drenching or foliar
spray with saponins from Acacia auriculiformis reduced root galling
by M. incognita (Roy et al., 1993).
3.5. Other compounds
Many volatile and non-volatile compounds are known to be
generated from decomposing organic amendments under either
aerobic or anaerobic soil conditions (Lewis and Papavizas, 1970;
Ponnamperuma, 1972; Gamliel and Stapleton, 1993). Sulfur-
containing compounds, such as CH3SH, (CH3)2S and (CH3)2S2, were
detected in soil amended with cabbage residues (Lewis and
Papavizas, 1970). Under anaerobic soil conditions, carbon dioxide,
ethylene, hydrogen, methane, organic acids, alcohols, dimethyl
sulfide and aldehydes may accumulate (Ponnamperuma, 1972;
Gamliel and Stapleton, 1993), and some of these are known to be
nematicidal. Except for the organic acids, which were covered above,
nematicidal activity of these compounds has not been thoroughly
studied. Cultivation and incorporation of pearl millet (Pennisetum
glaucum) hybrid cv. CFPM 101 was effective at controlling P.
penetrans on flue-cured tobacco (Bélair et al., 2004). In addition to its
poor host status for nematodes, the pearl millet cultivar contains
greater concentrations and amounts of sulfur-containing com-
pounds, which may play a role in nematode suppression. Among the
sulfur-containing compounds, hydrogen sulfide (H2S), generated
from flooded rice fields, was found to have nematicidal activity
(Rodrı́guez-Kábana et al., 1965). A decline in total nematode
populations was correlated with the increase in hydrogen sulfide
concentration in the soil water phase. Interestingly, hydrogen
sulfide was found to increase thermotolerance and lifespan of
Caenorhabditis elegans when exposed to the compound at a
concentration of 50 ppm in atmospheres (Miller and Roth, 2007).
4. Enhancement of antagonistic organisms
The idea of using antagonistic microorganisms to control plant–
parasitic nematodes was suggested almost 90 years ago (Cobb,
1920). Years later, Linford (Linford, 1937; Linford et al., 1938)
found that incorporation of organic amendments reduces popula-
tions of Meloidogyne spp. in the soil, probably by increasing the
population of antagonistic microorganisms. Several organic
amendments, some applicable in fields, others used only for
experimental purposes, were tested for how they affect nematodes
and nematode antagonists (Stirling, 1991). Fungi, bacteria and
predatory nematodes have been most studied in terms of
antagonism to plant–parasitic nematodes (Jatala, 1986; Stirling,
1991); however, other organisms, such as collembolans, enchy-
traeids, mites, protozoa, tardigrades and turbellarians, are also
known to attack nematodes (Jatala, 1986). An increase in
nematode-antagonistic organisms in amended soil is generally
thought to result from an increase in the number of free-living
nematodes (bacteriovorous and fungivorous), but reported uses of
 Y. Oka / Applied Soil Ecology 44 (2010) 101–115
specific organic amendments that are known to increase antag-
onistic organisms are scarce. Organic soils receive more organic
amendments than conventional agricultural soils, and these may
help antagonistic organisms become established and proliferate,
with a higher population density and diversity. One study showed
that the number of species of nematode-trapping fungi was higher
in organic than conventional soils, and that population densities of
some fungi were also higher in organic soil (Jaffee et al., 1998).
Number of antagonists is likely to exhibit a positive relationship
with nematode suppression in soil. Density-dependent parasitism
of some nematophagous fungi on a plant–parasitic nematode
(juveniles of Heterodera schachtii) was demonstrated (Jaffee et al.,
1993). Verticillium chlamydosporium, a fungal parasite of nematode
eggs and females, was also reported to become established and
survive in the organic soil, and another obligate parasitic fungus,
Hirsutella rhossiliensis, also infected and reproduced on M. hapla
(Vianene and Abawi, 2000).
Many studies have isolated potential antagonists from
amended soils, but it is difficult to define the specific role of each
in nematode suppression. Generally, these isolated organisms are
applied to nematode-infested soil with or without amendments to
estimate their potential as biological control agents (Stirling,
1991). Nematode suppression may also be induced by ‘‘non-
antagonistic’’ organisms. For example, fungivorous nematodes
(Aphelenchus avenae), which can be increased by organic amend-
ments and are not antagonists of plant–parasitic nematodes,
reduced plant infection with the plant–parasitic nematode M.
incognita, probably by competing for its ecological niche (Ishibashi
and Choi, 1991). Changes in microflora in amended soils can be
partly estimated by counting bacterial and fungal populations, or
by molecular methods, but the role of the total microflora in
nematode suppression, and specifying the main organisms
involved in the suppression, is very difficult (Stirling, 1991). Soil
environments most certainly have an effect on the changes in
antagonistic microorganism populations, but not enough informa-
tion is available. The following are examples of enhancement of
antagonistic organisms according to amendment types.
4.1. Plant residues
Cover crop and green manures are very popular organic
amendments for soil fertility and control of soilborne diseases.
Incorporation of plant residues generally increases the number of
free-living nematodes, but increases in specific nematode genera
may be affected by plant residue type (McSorley and Frederick,
1999), which in turn may affect antagonistic organisms, such as
predatory nematodes and parasitic fungi. Incorporation of
sunnhemp (Crotalaria juncea) to soil increased nematode-trapping
fungi, parasitic fungi on Rotylenchulus reniformis eggs, vermiform-
stage parasites, and bacterivorous nematodes more efficiently than
amendments with Brassica napus or Tagetes erecta (Wang et al.,
2001). As mentioned earlier, fungicidal and nematicidal com-
pounds in the latter plants were suggested to inhibit the increase in
populations of free-living nematodes, which in turn, inhibited the
development of organisms antagonistic to plant–parasitic nema-
todes.
An increase in the number of predatory nematodes is often
observed after amending soil with plant residues, probably as a
result of the proliferation of free-living nematodes as prey.
Application of neem leaf powder or sawdust increased the number
of predatory and free-living nematodes in the soil, while plant–
parasitic nematodes decreased (Akhtar, 1998). Another study
showed that amending soil with C. juncea increases the number of
bacterivorous, omnivorous, and predatory nematodes, but the
increased abundance of omnivorous and predatory nematodes was
not sufficient to suppress M. incognita (Wang et al., 2003).
107
Predatory nematodes from three orders, Dorylaimida, Mononchida
and Diplogasterida, may play a role in the suppression of plant–
parasitic nematodes (Bilgrami and Brey, 2005). Although several
small-scale experiments using cultured predatory nematodes
indicated their potential as biological control agents against
plant–parasitic nematodes (Cohn and Mordechai, 1974; Khan and
Kim, 2005; Bar-Eyal et al., 2008), their role in nematode control
under field conditions requires further study.
Crop rotation and incorporation can also change bacterial
populations in the rhizosphere. One study indicated that
rhizobacteria from the roots of antagonistic plants, such as velvet
bean, castor bean and rye, were mainly gram-negative genera,
whereas those isolated from soybean roots were mainly Bacillus
spp. A higher percentage of rhizobacteria isolated from the
antagonistic plants reduced nematode damage on soybean by H.
glycines and M. incognita compared to rhizobacteria isolated from
the soybean rhizosphere (Kloepper et al., 1992). The effect of
amending soil with plant residues on facultative bacterial
nematode parasites is not known, because such bacteria have
not been as well-studied as the facultative fungal parasites of
nematodes.
With respect to the effects of organic amendments, the most
studied nematode-parasitic microorganisms are probably the
fungi, especially facultative nematode-trapping fungi. Linford et
al. (1938) found that incorporation of chopped pineapple plants
reduces the population of root-knot nematodes, and suggested
that elevated populations of bacteria and bacterivorous nematodes
increase the number of nematode-trapping fungi, which in turn
attack the larvae of the root-knot nematode. However, Jaffee et al.
(1994) found that the number of bacterivorous and fungivorous
nematodes increases but parasitism of nematodes by Hirsutella
rhossiliensis usually decreases with the addition of wheat straw or
composted cow manure to a loamy sand naturally infested with H.
rhossiliensis. These results did not support the hypothesis that
organic amendments enhance parasitism of nematodes by H.
rhossiliensis. Influences of organic amendments on nematode-
trapping fungi and nematode suppression may also be highly
dependent on fungal species, and on the type and quantity of the
amended organic matter. Network-forming species, such as
Arthrobotrys spp., are generally more saprophytic, and show an
increase in their population after adding large quantities of alfalfa
to the soil, but this is not always accompanied by a reduction in
nematodes (Jaffee, 2004). On the other hand, the population
density and trapping of Dactylellina candidum, an adhesive knob-
forming fungus, were increased by smaller, but not larger
quantities of the amendment (Jaffee, 2004). Adhesive knob-
forming fungi are generally more parasitic or less saprophytic,
and their population is often influenced by the total nematode
population in the soil, while not being directly influenced by
nutrients from soil organic matter (Jansson and Nordbring-Hertz,
1980; Jaffee, 2006). Jaffee (2006) showed that the number of D.
candidum does not increase in alfalfa-amended soil if nematodes
are not present, whereas when nematodes are present, alfalfa
amendment increases the number of fungi. These results suggest
that organic amendments increase the bacterial population, which
supports population growth of bacterivorous nematodes, which in
turn supports the population growth of D. candidum, in contrast to
Arthrobotrys oligospora, which grows as a saprophyte on the
amendment rather than on nematodes. However, the relationship
between population density of the nematode-trapping fungi and
nematode population in the soil is not always negative, and the
reason for this is not clear. What is clear is that other aspects
should not be neglected when studying the effect of organic
amendments on nematophagous fungi, such as generation of
fungicidal compounds, population of natural enemies of the fungi,
and nematode-host ranges of nematophagous fungi. For example,
108 Y. Oka / Applied Soil Ecology 44 (2010) 101–115
enchytraeids and some microorganisms have been found to
contribute to the suppression of nematophagous fungi in field
plots (Jaffee et al., 1997).
4.2. Animal manure
Animal manure or compost is one of the most popular organic
amendments for soils. Aside from the toxic compounds generated
by manures in soil, nematode suppression may also be caused by
changes in the soil’s microfauna and microflora and increase in the
populations and activities of microorganisms that are antagonistic
to nematodes; however, a clear relationship among animal
manures, antagonistic microorganisms and nematode suppression
has never been demonstrated. Again, nematode suppression can be
highly affected by type and dose of the manure, as well as its
endogenous microflora. A few studies have reported on the
involvement of microorganisms in nematode suppression in soils
amended with animal manures. Population density of M. incognita
decreased linearly with increasing number of bacteria, which was
caused by increasing rates of chicken litter in the soil (Kaplan and
Noe, 1993). Nematode infection was lower on tomato planted in
soil amended with non-sterilized chicken litter than on that
planted in soil amended with sterilized chicken litter (Kaplan et al.,
1992). This result suggested that microorganisms in the chicken
litter are important for its nematode-suppressive effect.
Nematophagous fungi appear to use manures as a growth
substrate or ecological niche where free-living and animal-
parasitic nematodes are abundant. Spores of several nematopha-
gous fungi can survive in the digestive systems of ruminants,
horses, and pigs (Wolstrup et al., 1996), and their excrement can
therefore be a source of fungi. From 150 samples of sheep feces,
130 isolates of nematophagous fungi were recovered (Saumell et
al., 2000). More than 70% were predators, and Arthrobotrys and
Monacrosporium spp. predominated in the samples. The effect of
the isolated fungi on plant–parasitic nematodes was not studied;
however, fungi from the genuses Arthrobotrys and Monacrosporium
are known to parasitize several plant–parasitic nematodes (Al-
Hazmi et al., 1982; Khan et al., 2006). A difference in manure type
resulted in population growth of nematophagous fungi. The
number of such fungi increased in soil amended with cow and
chicken manure although these increases were more pronounced
when the soil was treated with the latter (Wachira et al., 2009). In
the same soils, the number of free-living and predatory nematodes
also increased, whereas that of plant–parasitic nematodes
decreased. Similar results were reported by Dackman et al.
(1987). However, application rates should be considered because
manures can suppress soil fungi if applied in high amounts, due to
the presence of fungicidal compounds such as ammonia (Jaffee et
al., 1994).
4.3. Chitinous materials
Chitinous materials have attracted special attention for their
control of nematodes and soilborne fungal diseases because chitin
is present in nematode egg shells as well as in the cell walls of most
plant-pathogenic fungi. Soil application of these materials
increases the number of chitinolytic microorganisms and chitinase
activity in the soil, which in turn has an adverse effect on
nematodes and fungi (Mian et al., 1982; Spiegel et al., 1987;
Gotlieb et al., 2003; De Jin et al., 2005). Amending soil with
chitinous materials resulted in nematode suppression via at least
two different mechanisms. First, nematode suppression appeared
not long after amendment application due to the toxic nitrogenous
compounds, mainly ammonia and nitrous acid (Spiegel et al.,
1987). Second, suppression that lasted even after depletion of the
toxic nitrogenous compounds or only appeared a few months later
might be caused by the increased number and activity of
antagonistic organisms (Rodrı́guez-Kábana et al., 1987; Spiegel
et al., 1987; Hallmann et al., 1999; De Jin et al., 2005). Application
of chitinous material has been shown to increase the number of
chitinolytic microorganisms, such as bacteria, fungi and actino-
mycetes, as well as chitinase activity in the soil, and to reduce
plant–parasitic nematodes and fungi (Mian et al., 1982; Rodrı́guez-
Kábana et al., 1983; Spiegel et al., 1987; Hallmann et al., 1999).
Among the changes in microflora, the number of actinomycetes
was particularly increased more than 1 month after amending with
chitinous material (Spiegel et al., 1987). Some microorganisms
isolated from chitin-amended soil are known as nematode egg
parasites (Godoy et al., 1983; Rodrı́guez-Kábana et al., 1984) or
have been tested for their biocontrol efficacy against nematodes
(Spiegel et al., 1991; Cronin et al., 1997; Tian et al., 2000). Among
these, the newly identified bacterium Telluria chitinolytica (=Pseu-
domonas chitinolytica) showed potential for root-knot nematode
control (Spiegel et al., 1991). Bacterial communities colonizing the
rhizosphere and endorhiza of cotton plants were greatly modified
by chitin amendment, which reduced infestation of cotton by M.
incognita (Hallmann et al., 1999). Several bacterial species were
found only in chitin-amended soils and rhizospheres, and some
endophytes, such as Burkholderia cepacia, were dominant in roots
of cotton plants grown in the amended soil, but not in control
plants (Hallmann et al., 1999). It was not clear how these changes
affect nematode infestation of the plants, but the results indicated
that the nematode suppression could be associated not only with
microbial changes in the soil and rhizosphere, but also with
changes in the bacterial community within the plant tissue.
4.4. Compost
Compost is a very important soil component, especially in
organic farming systems. Composts are generally prepared from
agroindustrial wastes, such as tree bark, animal wastes and green
wastes. They are used to provide the soil with nutrients and
organic matter and to improve the soil’s structure. Another merit of
using compost is a reduction in disease incidence. Some kinds of
compost have been reported to suppress soilborne pathogens in
the genera Pythium, Phytophthora, Fusarium and Rhizoctonia
(Hoitink et al., 1997). Certain microorganisms in composts are
thought to play a role in plant disease control. Fungal genera, such
as Trichoderma, Penicillium and Aspergillus, bacterial genera,
Bacillus, Pseudomonas and Pantoea, and actinomycetes are antag-
onistic to some soilborne disease-causing fungi (Hoitink and
Boehm, 1999). Some of these microbial genera are also known to be
suppressive to nematodes (Sharon et al., 2001; Kluepfel et al.,
2002; Kokalis-Burelle et al., 2003; Mekete et al., 2009). In some
experiments, composts and raw sewage sludge showed activity
against root-knot nematodes and root-lesion nematodes (Marull
et al., 1997; LaMondia et al., 1999; Everts et al., 2006) but in others,
composts affected nematodes only slightly, if at all (McSorley and
Gallaher, 1995, 1996). In a long-term experiment, application of
compost increased total yields of potato tubers and grain yields of
barley, but the impacts on P. penetrans, M. hapla and Heterodera
trifolii varied, usually increasing their population levels in the soil
(Kimpinski et al., 2003). Along with biotic factors, abiotic factors
are thought to be involved in disease suppression (Hoitink et al.,
1997). However, the mechanisms underlying composts’ suppres-
sion of plant–parasitic nematodes have not been studied as
thoroughly as their effects on fungal diseases. Specific nematode-
antagonistic microorganisms have not been isolated from nema-
tode-suppressive composts, and two studies indicated that
nitrogenous compounds, rather than microorganisms, contribute
to the nematode suppression (Oka and Yermiyahu, 2002; Raviv et
al., 2005). Composts based on cattle manure were suppressive to
 Y. Oka / Applied Soil Ecology 44 (2010) 101–115
M. javanica in pot and in-vitro experiments. Chemical analysis of
the composts and leachates from the soils suggested that high
electrical conductivity (EC) values and high concentrations of
nitrogen, especially N-NH3/NH4+ rather than N-NO3, suppressed
the nematodes. Another example of nematode suppression by
abiotic factors is the use of olive mill waste compost, which
contains nematicidal compounds, and has been suggested for use
as a biopesticide (Cayuela et al., 2008).
4.5. Other materials
Since the main constituent of the nematode cuticle is collagen,
this structural protein was used as a soil amendment based on the
hypothesis that microorganisms that can degrade and utilize this
protein as a nutrient source will increase in number and activity in
the soil, and nematodes will be suppressed due to direct
(parasitism) or indirect effects, such as elevated soil collagenase
activity (Galper et al., 1990). Root galling of M. javanica on tomato
was reduced by amending soil with collagen, although the
concentration of ammonia generated from the collagen in the soil
was below that which is lethal to nematodes (Galper et al., 1990).
Increased proteolytic activity in the amended soil was suggested to
be involved in the nematode suppression. Indeed, treatment of
nematode juveniles with collagenase greatly reduced their
infectivity. In a subsequent study, a collagenolytic fungus,
Cunninghamella elegans, isolated from the collagen-amended soil,
reduced the root-galling index of tomatoes by 90% when the
collagen amendment was supplemented with the fungus, whereas
collagen without the fungus reduced galling by 70% (Galper et al.,
1991). Culture filtrates of C. elegans immobilized M. javanica
juveniles and inhibited egg hatch. However, the nematicidal effect
of the culture filtrates varied among nematode species: it was
effective on Rotylenchulus reniformis and Xiphinema index, but less
effective on Anguina tritici and nearly ineffective on D. dipsaci. The
results suggested differences in cuticle structure among the
nematodes. Some nematode-trapping fungi, such as Arthrobotrys
amerospors, are also known to produce collagenases, which may be
used during infection (Schenck et al., 1980). The fungus C. elegans
also showed keratinolytic activity (Galper et al., 1991). Keratin is
found in the cuticle of some animal-parasitic nematodes, in
addition to collagen (Bird, 1971). Although this structural protein
is not known in plant–parasitic nematodes, the external cortical
layer of plant–parasitic nematodes resembles keratin in some
respects (Bird, 1971). Keratinous materials, such as feather and
horn meal, were used as amendments for the control of root-knot
nematodes (Khan and Saxena, 1997; Oka et al., 2007a). These
materials are often used in organic farms as slow-release fertilizer.
Generation of ammonia from feather meal, rather than enhance-
ment of keratinolytic antagonists, was suggested to be the
nematicidal factor in nematode suppression (Oka et al., 2007a).
The integration of oil cakes, and bone and horn meals with the
fungus Paecilomyces lilacinus resulted in increased plant growth
and reduced population buildup of nematodes and root galls (Khan
and Saxena, 1997), although P. lilacinus is not a keratinolytic
fungus, but produces proteases and is known as a nematode
parasite (Jatala, 1986).
5. Increase in plant tolerance/resistance
Some chemical compounds, such as salicylic acid, b-aminobu-
tyric acid and phoshite, have been reported to induce resistance in
plants to nematodes (Oka et al., 1999, 2007b). Addition of organic
amendments or those enriched with microorganisms somehow
makes plants more tolerant or resistant to nematodes. Induced
resistance in plants caused by chemicals from microorganisms has
been mostly studied against fungal, bacterial and viral pathogens,
109
and several resistance mechanisms in plants have been indicated
(Bostock, 2005). There are two possible causes of plant tolerance or
resistance brought on by organic amendments: development of
specific microorganism inducers and exposure to natural com-
pound inducers.
5.1. By microorganisms
Rhizobacteria that increase plant growth and/or plant resis-
tance are termed ‘‘plant growth-promoting rhizobacteria’’ (PGPR).
Induced resistance caused by such bacteria is termed systemic
acquired resistance (Durrant and Dong, 2004). Some reports have
indicated that the use of PGPR in seedling media improves plant
growth and occasionally reduces damage caused by soilborne
diseases, including root-knot nematodes. These rhizobacteria were
mainly Bacillus and Pseudomonas spp. (Kluepfel et al., 2002), and
are known to induce systemic resistance to several diseases (Van
Loon et al., 1998). Root galls caused by M. incognita on pepper and
muskmelon were reduced by some strains of PGPR (Kokalis-
Burelle et al., 2002, 2003), and damage on coffee plants by M.
incognita was reduced by endophytic species of Bacillus, such as B.
pumilus and B. mycoides (Mekete et al., 2009). Penetration of potato
roots by Globodera pallida was reduced by systemic resistance
induced by rhizobacteria Agrobacterium radiobacter, Bacillus
sphaericus or Rhizobium etli (Hasky-Günther et al., 1998; Reitz
et al., 2000). Heat-killed bacterial cells were also effective in
resistance induction (Reitz et al., 2000). These bacteria are
expected to be influenced by organic amendments, although
relationships among organic amendments, bacteria and plant
resistance to nematodes have not yet been revealed.
Similar to bacterial inducers, some fungi, mainly fungal
endophytes, increase plant resistance to nematodes (Sikora et
al., 2008). The presence of the fungal endophyte Neotyphodium
coenophialum in tall fescue confers resistance to some plant–
parasitic nematodes (Timper et al., 2005). A non-pathogenic
Fusarium sp. was reported to play a role in resistance to root-knot
nematodes in tomato (Hallmann and Sikora, 1994; Dababat and
Sikora, 2007). Trichoderma spp. have been developed as a
biocontrol agent for the control of soilborne fungi, such as Pythium
spp., Rhizoctonia solani, Fusarium spp. and Sclerotium rolfsii (Chet,
1990), and they are also known to control nematodes (Sharon et
al., 2001; Sahebani and Hadavi, 2008). Trichoderma spp. are
dominant in tree bark composts, and their role in disease
suppression has been suggested (Nelson et al., 1983; Hoitink
and Boehm, 1999). In greenhouse experiments, soil treatment with
T. harzianum peat-bran preparations reduced root galling and
increased top fresh weight of tomatoes grown in M. javanica-
infested soil (Sharon et al., 2001). The fungus showed the ability to
infect M. javanica eggs and juveniles in the laboratory (Sharon et
al., 2001). In addition to its direct parasitism of nematodes,
Trichoderma-induced resistance in plants to nematodes has been
suggested to be due to its induction of proteins involved in plant
defense (Sahebani and Hadavi, 2008), similar to its induction of
plant resistance to foliar diseases (De Meyer et al., 1998; Yedidia et
al., 1999).
The mechanisms underlying reduction of nematode infection or
induced resistance in plants by these microorganisms are not
clearly understood, but they may produce nematicidal compounds
(antibiotics), inhibit nematode orientation towards the host roots
by modifying root exudates, physically occupy nematodes’
infection or feeding sites, or elicit the plant defense systems as
in systemic acquired resistance (Durrant and Dong, 2004).
Metabolites of a non-pathogenic F. oxysporum strain, which was
isolated from tomato roots and increased resistance to M. incognita,
were toxic to the nematode and some soilborne fungi (Hallmann
and Sikora, 1996). These inducers of nematode resistance may be
110 Y. Oka / Applied Soil Ecology 44 (2010) 101–115
applied in the nursery as a component of seedling growth media to
protect plants from nematode infection and promote plant growth
in the field (Kokalis-Burelle et al., 2002, 2003).
5.2. By natural compounds
Nematode infestation was reduced by applying seaweed
extracts, which were not in and of themselves nematicidal, by
soil-drenching (Featonby-Smith and van Staden, 1983; De Waele
et al., 1988; Crouch and van Staden, 1993; Wu et al., 1997). These
extracts were prepared from the seaweed species Ascophyllum
nodosum and Ecklonia maxima. Among the many effects of seaweed
preparations on soils, microorganisms and plants, they have been
suggested to induce resistance to abiotic and biotic stresses,
including nematode infections (Khan et al., 2009). Resistance to
nematodes in treated plants may be caused by alteration of their
auxin-to-cytokinin ratio. The specific constituents of the extracts
involved in nematode resistance are not fully understood. However,
betains, which have been found in alkaline extracts of the brown alga
A. nodosum, reduced infection of tomato plants with root-knot
nematodes (Wu et al., 1997). Betains were reported to increase
chlorophyll content, work as a nitrogen source, and serve as an
osmolyte and compatible solute that alleviates osmotic stress in
plants (Khan et al., 2009). However, it is not clear how these
compounds and the extracts increase plant resistance to nematodes.
Some constituents of plant extracts have also been suggested to
increase resistance or tolerance to nematodes. Sincocin, a commer-
cial liquid concentrate derived from plant extracts and fatty acids,
reduced a population of Tylenchulus semipenetrans on citrus roots
(Osman and Salem, 1995). Phenols released from neem oil cake into
amended soil were suggested to increase resistance of tomato plants
to M. javanica due to the higher phenol content in their roots
(Sitaramajah and Singh, 1978). The phenolic compounds from the oil
cakes also reduced nematode attraction to tomato roots (Singh et al.,
1983). It is not clear, however, whether application of organic
amendments with a high content of phenolic compounds, such as
spent coffee grinds and olive mill waste, directly affects nematodes
or increases plant resistance (Mian and Rodrı́guez-Kábana, 1982;
Cayuela et al., 2008), because several phenolic compounds possess
nematicidal activity (Chitwood, 2002).
6. Physical changes in the soil
Organic amendments may change the soil’s physical properties,
which in turn may affect adversely nematode behaviors such as
hatching, movement and survival. These soil changes include pH,
salinity and EC, carbon dioxide and oxygen concentrations, redox
potential and soil structure. Nematodes are generally tolerant to a
wide range of pHs (Khanna et al., 1997; McSorley, 1998), but acidic
and alkaline soil pH, caused by soil amendments (generation of
ammonia and its nitrification or organic acids), may contribute to
nematode suppression with no connection to pH-dependent
nematicidal compounds (i.e. ammonia, nitrous acid and volatile
fatty acids). Acidification of soil with hydrochloric acid to pH 3.5
reduced Tylenchorhynchus spp. by 70% under aerobic conditions,
and by 80% under anaerobic conditions (McElderry et al., 2005).
Alkalization with cement kiln dust to pH 10 did not kill juveniles of
M. javanica, but it did at pH 11 (Oka et al., 2006b). However, the
effect of soil pH appears to vary among nematode life-history
groups (Ruess and Funke, 1992).
Amendments also affect salinity, EC and osmotic pressure of the
soil water film in which nematodes exist. Soil-inhabiting
nematodes are generally capable of tolerating high osmotic
pressures, and rarely experience conditions under which their
movement might be inhibited (Van Gundy, 1965). However,
frequent addition of animal manure to soil may increase soil
salinity and EC (Poudel et al., 2001; Yao et al., 2007), which may
adversely affect nematodes. Water extracts of soil amended with
cow manure-based compost killed juveniles of M. javanica,
probably due to high EC and ammonium concentrations, whereas
eggs were less affected (Oka and Yermiyahu, 2002). Egg hatching of
M. javanica has been reported to decrease with increasing
concentration of electrolytes (NaCl, CaCl2, KCl) (Dropkin et al.,
1958). A study showed that adding sucrose or glucose to soil at
concentrations of 1–5% (w/w) caused direct nematode death in less
than 24 h, probably by high osmotic pressure (Feder, 1960).
Application of granular sucrose or its solution reduced infection of
tomato plants with root-knot nematodes (Santiago et al., 2005). In
addition to the direct osmotic effect of high-salinity environments
on nematodes, they can be indirectly affected by such physical
changes. Development of M. incognita in tomato roots was
inhibited by increased salinity (Edongali et al., 1982). An example
of the indirect effect of soil-moisture osmotic pressure on
nematode suppression is provided by Criconemella xenoplex, which
was more susceptible to infection by the fungal parasite Hirsutella
rhossiliensis at high osmotic tensions of 30–300 kPa than in tap
water (Jaffee and Zehr, 1983).
Carbon dioxide concentration increases and oxygen concentra-
tion decreases in soil during organic-matter degradation due to
microbial activity. Most soil-inhabiting nematodes are able to
tolerate such conditions by reducing their normal oxidative
metabolism level and switching to the fermentative pathway of
facultative anaerobiosis (Womersley et al., 1998). Nevertheless,
low or no oxygen and increased carbon dioxide are not suitable for
nematode behaviors, including hatching, movement and infection
(Wong and Mai, 1973), and such changes are expected to be more
extreme in amended soil tarped with plastic sheet which, as
already mentioned, is an effective control method for nematodes
and fungal diseases (Blok et al., 2000; Ploeg and Stapleton, 2001;
Taba et al., 2006; Oka et al., 2007a). Low redox potential in
amended plus tarped soil causes the generation of several
nematicidal and fungicidal compounds, including organic acids
and aldehydes, which accumulate in the soil, similar to the
situation in flooded soils (Ponnamperuma, 1972). However, the
direct effects of low oxygen or high carbon dioxide concentrations
and low redox potential in nematode suppression in amended soils
are unknown. Some physical changes, which cause stress to
nematodes in amended soil, are also known to induce nematodes
to become quiescent or cryptobiotic via anoxybiosis (low oxygen
concentration) and osmobiosis (osmotic shock) as a survival
strategy (Womersley et al., 1998).
Another factor which may play a role in nematode suppres-
sion in amended soils is soil structure. Aggregation of soil
particles is one example of a change in structure in amended
soils. Soil pore size is known to affect nematode habitat and
movement, and it changes with soil aggregation. The neck
diameters of the habitable pore space for nematodes have been
estimated at 30–90 mm, based on a correlation between pore-
size distributions and nematode biomass (Hassink et al., 1993).
Higher numbers of plant-parasitic and free-living nematodes
were found in aggregates with diameters of 50–200 mm, which
were suggested to provide inter-aggregate pores of 50–300 mm
in diameter (Quénéhervé and Chotte, 1996). These niches may
also serve as a survival site for nematodes (Sano and Nakasono,
1997). Smaller and larger pore sizes reduced nematode mobility
(Wallace, 1958; Otobe et al., 2004). Larger pore size as a result of
soil aggregation may enable large natural enemies, such as
collembolans, enchytraeids, mites, tardigrades, turbellarians and
predatory nematodes, to move in the soil and prey on nematodes.
Again, no study has been conducted to verify the effect of
structural changes in amended soils on the movement, infection
or survival of plant–parasitic nematodes.
 Y. Oka / Applied Soil Ecology 44 (2010) 101–115
7. Outlook
Due to the restrictions governing the use of nematicides and soil
fumigants, environmentally friendly or sustainable methods have
taken on a more important role in control strategies for plant–
parasitic nematodes. A large variety of organic amendments have
been used to control nematodes under many situations and on
many scales, from trials in pots to commercial farms. Several
organic amendments/preparations have been commercially
released as nematicides, although their control efficacies are
generally low, or even non-existent (Crow, 2005). No organic
amendment alone appears to be able to replace nematicides or soil
fumigants, but integration of this method with others, such as the
use of resistant cultivars or soil solarization, will improve its
control efficacy and yield a more economically acceptable level of
control.
Chemical soil fumigants are effective for a relatively wide range
of soilborne diseases; however, their biocidal effect may destroy
biological balances or equilibrium in the soil. This is likely to cause
a ‘biological vacuum’, whereby pathogens can recolonize the soil
even faster than untreated soils (Kreutzer, 1965). Frequent
application of nematicides based on organophosphates and
carbamites or soil fumigants results in the buildup of bacterial
populations, which can degrade these chemicals in a short time
and reduce their nematicidal activity in the soil (Ou, 1998; Moens
et al., 2004). As already noted, efficacy of organic soil amendments
in nematode control, on the other hand, is generally lower than
that of chemicals, and the integration of other control methods is
required to achieve the desired control levels. However, the
nematode suppressiveness obtained by organic amendments
occasionally lasts for longer periods, probably due to changes in
biological balances and increased microbial activity in the soil
which are not amenable to population buildup of the plant–
parasitic nematodes.
Although organic amendments have been used for the control
of soilborne diseases since ancient times, the mechanisms
governing their ability to suppress nematodes are complex and
not well understood—not only due to the variety of amendment
types, but also to the variety of soil environments. However, if even
one of these nematode-suppressive mechanisms were to be
elucidated or even suggested, improvement of the suppressive
effect would be theoretically possible via manipulation of the soil
environment, such as its alkalization to increase the concentration
of generated ammonia, or its acidification to increase the
concentration of nitrous acid or short-chained volatile fatty acids.
In point of fact, several experiments have demonstrated that this
strategy for increasing control efficacy is not only theoretically
possible but also realistic, as well as practical and feasible under
certain circumstances. We have to remember that plant–parasitic
nematodes are only one group of soilborne pathogens: other
pathogens are also present in most agricultural fields. Combina-
tions with other methods for other soilborne pathogens are
essential for agricultural practice. Fortunately, some of the
nematode control methods that use organic amendments are also
effective at controlling other soilborne diseases, mainly fungal
pathogens.
In contrast to nematicidal chemicals released from amend-
ments, the role of microbial changes following these amendments’
application to the soil has not been well studied, and remains
unclear. An increase in nematode-antagonistic microorganisms,
mainly predators and parasites, plays an important role in
nematode suppression. In fact, antagonists of nematodes, includ-
ing fungal and bacterial parasites, have been found in ‘naturally
suppressive soils’ (Kim and Riggs, 1991; Weibelzahl-Fulton et al.,
1996; Olatinwo et al., 2006). Such antagonists have great potential
as biological agents for nematode control, and combinations of
111
bioagents and organic amendments that may support their
establishment in the soil and their release of nematicidal
compounds during degradation are likely to improve control
efficacy. Non-antagonistic microorganisms that build up after
amendment application, which cannot kill nematodes directly but
may affect plant physiology or nematode behavior, also appear to
play an important role. Such organisms may be applied to
seedlings’ root systems in nurseries as biological control agents.
In fact, several attempts in this direction have been made to protect
crop roots from nematodes and other pathogens (Kokalis-Burelle
et al., 2002, 2003; Kloepper et al., 2004).
Returning organic materials to the soil, especially agricultural
wastes and agroindustrial byproducts, contributes to reducing
the amount of waste to be treated, and seems to support
environmental protection; however, we have to remember that
some organic materials will contaminate the environment and
damage crops if they are not applied appropriately. The most
popular such amendment is uncomposted animal manure. Odor
pollution, nitrate leaching to the groundwater, dispersal of
animal pathogens, and crop damage due to high nitrogen content
or salinity, are the most common examples of potential damage.
A better understanding of control mechanisms, nematode control
efficacy and environmental impacts by organic amendments
requires broad knowledge in phytochemistry, soil microbiology,
soil chemistry and ecology, in addition to nematology. A
multidisciplinary research approach, involving a collaboration
on the different aspects of amendments’ effects, is our best hope
of successfully achieving the research target, and helping in the
development of nematode control methods, not only for organic
or sustainable farming systems but also for conventional
farming.
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