1104 NEMATICIDES

Smith, A. E. and Secoy, D. M., Plants used for agricultural pest soil or within plant roots, delivery of a chemical to the
control in western Europe before 1850, Chem. Ind. 12–17 immediate surroundings of a nematode is difficult. The
(1981). outer surface of nematodes is a poor biochemical target
Stoll, G., Natural Crop Protection Based on Local Farm Resources and is impermeable to many organic molecules. Deliv-
in the Tropics and Subtropics, Verlag Josef Margraf, Aichtal, ery of a toxic compound by an oral route is nearly
1986, pp. 1–186. impossible because most phytoparasitic species ingest
Ujváry, I., Pest control agents from natural products, in material only when feeding on plant roots. Therefore,
R. I. Krieger, ed., Handbook of Pesticide Toxicology, 2nd ed., nematicides have tended to be broad-spectrum toxicants
Academic Press, San Diego, 2001, pp. 109–179 (a thorough
possessing high volatility or other properties promot-
work on the chemistry, biochemistry and toxicology of natural
products used in pest control).
ing migration through the soil. The resulting record of
less-than-perfect environmental or human health safety
Wink, M., Schmeller, T., and Latz-Brüning, B., Modes of action
of allelochemical alkaloids: Interaction with neuroreceptors, has resulted in the widespread deregistration of sev-
DNA, and other molecular targets, J. Chem. Ecol. 24: eral agronomically important nematicides (e.g., ethylene
1881–1937 (1998) (a comprehensive paper on the subject). dibromide and dibromochloropropane). The most impor-
Pest Management Science 56: 649–723 (2000) (this Natural tant remaining fumigant nematicide, methyl bromide,
Product/Biocontrol special issue of the journal contains a faces immediate severe restrictions and future prohi-
series of articles on the chemistry, regulation, use, and bition because of concerns about atmospheric ozone
environmental fate of a broad range of biopesticides). depletion (2).
This review focuses on the chemical compounds
presently used against plant-parasitic nematodes and the
NEMATICIDES compounds with the greatest likelihood to replace some of
the current problematic compounds. Chemical control of
DAVID J. CHITWOOD
nematodes of veterinary or medical importance is achieved
USDA-ARS
through use of several compounds useful in management of
Beltsville, Maryland
several types of vermiform parasites besides nematodes.
In general, mammalian anthelmintics are poorly suited
Nematodes are nonsegmented, bilaterally symmetric
as agronomic nematicides because of lack of mobility in
worm-like invertebrates that possess a body cavity and
soil, expense, or other undesirable properties. Readers
a complete digestive system but lack respiratory and
curious about mammalian anthelmintics should refer to
circulatory systems. The body wall is composed of a
several excellent reviews (3–5). The mode of action of
multilayered cuticle, a hypodermis with four longitudinal
some mammalian nematicides is briefly discussed in this
cords, and internal musculature. The most conspicuous
review.
feature of the nervous system is the nerve ring near the
nematode pharynx. The so-called excretory system has
never been associated with removal of metabolic wastes; AGRICULTURAL IMPACT OF NEMATODES
instead, it functions in osmoregulation or in the secretion
of compounds essential to the life history of the nematode, As with damage caused by other crop pests and pathogens,
depending on the species and the developmental stage. the extent of crop losses caused by nematodes is a topic of
The digestive and reproductive systems constitute much debate. The most comprehensive estimate was obtained
of the body contents. in a 1986 survey incorporating the responses of 371
Most nematode species are ‘‘free-living’’; i.e., they nematologists in 75 countries (6). Estimates of nematode
feed on microorganisms in water and soil. A smaller damage to specific crops ranged from 3.3% to 20.6%,
number of species are ubiquitous parasites of animals or with a mean of 12.3%. Annual production losses at the
plants. Indeed, Nathan A. Cobb (1), the father of American farm gate (in year 2000 dollars) were $121 billion globally
nematology, stated in 1914: and $9.1 billion in the United States. Developing nations
reported greater yield loss percentages than did developed
If all the matter in the universe except nematodes were countries.
swept away, our world would still be recognizable, and if,
Figures for mean crop losses can be deceptive;
as disembodied spirits, we could then investigate it, we
yield reduction in specific crops can exceed 75% in
should find its mountains, hills, vales, rivers, lakes, and
oceans represented by a film of nematodes. The location some locations (7). More typically, growers are forced
of towns would be decipherable, since for every massing of to select less profitable crops. In addition to directly
human beings there would be a corresponding massing of causing crop losses, nematodes can vector many plant
certain nematodes. Trees would still stand in ghostly rows viruses or create wounds that allow the entry of other
representing our streets and highways. The location of the root pathogens. Several nematodes are major pests of
various plants and animals would still be decipherable, and quarantine importance and interfere with free trade of
had we sufficient knowledge, in many cases even their species several agricultural commodities.
could be determined by an examination of their erstwhile
nematode parasites.
SPECIFIC NEMATICIDES: AN INTRODUCTION
The development of chemical controls for plant-parasitic
nematodes is a formidable challenge. Because most phy- Although the discovery of nematicidal activity in a
toparasitic nematodes spend their lives confined to the synthetic chemical dates from the use of carbon disulfide
 NEMATICIDES 1105

as a soil fumigant in the second half of the nineteenth trans isomer was completely ineffective against the potato
century, research on the use of nematicides languished cyst nematode Globodera rostochiensis (13).
until surplus nerve gas (chloropicrin) became readily
available following World War I (8). In the 1940s, the Ethylene Dibromide
discovery that D-D (a mixture of 1,3-dichloropropene and Once the most abundantly used nematicides in the world,
1,2-dichloropropane) controlled soil populations of phy- use of EDB was prohibited in the United States in
toparasitic nematodes and led to substantial increases 1983 because of groundwater contamination (8,10). It was
in crop yield provided a great impetus to the develop- available in liquid formulations and is regarded as a
ment of other nematicides, as well as the growth of the probable human carcinogen.
science of nematology. Subsequently, other halogenated
hydrocarbons and other volatile compounds were devel- 1,2-Dibromo-3-Chloropropane
oped as nematicidal soil fumigants. In the 1960s, a new
Liquid formulations of this fumigant with substan-
generation of nematicides was introduced—carbamates
tial nematode-specific activity were once popular. The
and organophosphates that served as contact nematicides,
compound was notable because of its usefulness in post-
devoid of fumigant activity. Many of the carbamates and
plant applications. The discovery that over one-third of
organophosphates are systemic within plants, but only
the male workers at a DBCP manufacturing plant in Cal-
one contact nematicide has registered systemic nematici-
ifornia were sterile led to the immediate 1977 prohibition
dal activity. For most systemics, the high concentrations
of its use in the United States, except for usage in pineap-
needed to retard nematode development within plant roots
ple production (14). Sterility problems were also reported
is not likely to occur under field conditions (9).
among some DBCP applicators (14). All uses were prohib-
Most soil nematicides are also registered as insecticides
ited in the late 1980s. DBCP is classified as a possible or
or fungicides and are discussed in greater detail
probable human carcinogen.
elsewhere in this volume. This broad-spectrum activity
is a result of the difficulty in discovering or designing Methyl Bromide
compounds capable of movement through the soil. In
addition, the small size of the commercial market for Methyl bromide is a broad-spectrum fumigant toxic to
nematicides in comparison to other pesticides dictates nematodes. In 1997, methyl bromide was the fourth most
that nematicide discovery is often an appendage to commonly used pesticide in the United States (11). It
research programs pursuing controls for other organisms. is agronomically useful against soil fungi, nematodes,
Compounds included in the following compilation of insects, and weeds. The Montreal Protocol, an interna-
chemical nematicides are not necessarily registered for tional treaty regulating the use of ozone-depleting sub-
usage in the United States or elsewhere, particularly when stances, mandates the elimination of methyl bromide use
viewed through their ever-changing regulatory context. in developed countries by 2005. Under a 1999 amendment
to the Clean Air Act, the United States phaseout of usage
will not be more restrictive than that mandated by the
FUMIGANTS Montreal Protocol. Research pursuing the development of
nematicidal methyl bromide alternatives has been inten-
D-D sive, but no single compound appears likely to substitute
This mixture of 1,2-dichloropropane and 1,3-dichloropro- for it. Methyl bromide is used as a gas; because of its
pene had widespread use as an effective nematicide until lack of odor, small amounts of chloropicrin are often added
problems with groundwater contamination resulted in its as an indicator of exposure to applicators and are often
withdrawal from use in 1984. The 1,2-dichloropropane required by specific governmental agencies, such as the
component was relatively inactive as a nematicide at state of Florida. Methyl bromide is the fastest moving
concentrations used in agricultural fields. fumigant in soils, followed by chloropicrin, 1,3-D, EDB,
methyl isothiocyanate, and DBCP (15).
1,3-Dichloropropene
Chloropicrin
Because of the relative lack of nematicidal activity
in 1,2-dichloropropane and the desire to eliminate One of the oldest soil fumigants, chloropicrin’s primary
groundwater contamination by a compound not useful agricultural use in soils is as a fungicide, although it does
for nematode control, 1,3-D became a highly successful have herbicidal and nematicidal activity. It is often added
nematicide. Although it also has fungicidal activity and to 1,3-D formulations in order to increase their fungicidal
insecticidal activity against wireworms in particular, the activity. The compound is acutely toxic and is used in liquid
primary use of the compound is as a nematicide. On a formulations. In 1997, it was the 25th most abundantly
weight basis, 1,3-D is the sixth most abundantly used used U.S. pesticide (11).
pesticide in the United States (11); 1,3-D is classified as
Metam Sodium, Dazomet, and Methyl Isothiocyanate (MITC)
a possible or probable human carcinogen. Commercial
formulations are liquids and contain two isomers. In Metam sodium is a soil fumigant used to control
one series of experiments, aqueous trans-1,3-D was nematodes, fungi, insects, and weeds; it is the third
60% as toxic as the cis isomer, whereas in the vapor most commonly used U.S. pesticide (11). When applied
phase, trans-1,3-D was 90% as toxic as cis-1,3-D (12). In to soils, metam sodium is converted to MITC, which is
laboratory experiments simulating field situations, the the active biocidal agent. MITC is no longer registered for
1106 NEMATICIDES

use as a soil pesticide in the United States, except as a lily (20). Oxamyl is widely used throughout the world and
wood preservative. Metam sodium and related compounds is less persistent in soil than is aldicarb (8).
have provided excellent control of nematodes in some
circumstances but not in others (8,16,17). Dazomet is
ORGANOPHOSPHATES
one of the few compounds with activity as a fumigant
that is supplied as a granular formulation. Research While this review is being written, the U.S. EPA is
on the use of isothiocyanates as nematicides began actively reviewing the uses of all organophosphates. It
in the 1930s (18). Several brassicaceous plants contain is possible that several of the following compounds will
nematicidal isothiocyanates or glucosinolates that release face mandatory or voluntary withdrawals from use in the
isothiocyanates when incorporated into soils (19). United States.
Sodium Tetrathiocarbonate
Ethoprop
Sodium tetrathiocarbonate is more recently registered
preplant soil fumigant active against fungi, insects, Introduced in the 1960s, ethoprop is a nonsystemic
and nematodes. It is supplied as a liquid formulation insecticide/nematicide. The mobility of ethoprop in soil
and may be applied via drip or surface irrigation. and its half-life are strongly dependent on soil organic
Sodium tetrathiocarbonate rapidly degrades in soil into matter (21). It is not known to be carcinogenic and is
carbon disulfide, sodium hydroxide, hydrogen sulfide, and available as granules or emulsifiable concentrates.
sulfur. Carbon disulfide is the active principle. Although
Fenamiphos
carbon disulfide has a long history as a fumigant, its
flammability is legendary. Carbonates and sulfates are the Also introduced in the 1960s, fenamiphos does have some
terminal degradation products. Unlike other commonly systemic insecticidal activity. It is widely used as a
used fumigants, sodium tetrathiocarbonate does not nematicide. Like ethoprop, it is strongly adsorbed onto
readily move through soil air and requires a high level organic matter. It is acutely toxic but not shown to be a
of soil moisture when applied in order to be distributed carcinogen.
throughout the soil.
Cadusafos
CARBAMATES This nonsystemic organophosphate not registered for
U.S. usage is used to control nematodes and soil
Aldicarb insects on bananas and other crops in several coun-
Like most other carbamate nematicides, aldicarb was tries. The U.S. EPA has granted tolerances for cadusafos
introduced in the 1960s. It is active against a wide variety in imported bananas, where it provides excellent con-
of nematodes (as well as insects and mites) and is useful in trol of the burrowing nematode, Radopholus similis (22).
a variety of soil types throughout the world (8). Aldicarb is Cadusafos reportedly possesses reduced risk for contami-
available in granular formulations and possesses systemic nating groundwater and provided good control of the citrus
activity. Aldicarb, carbofuran, and oxamyl are highly toxic nematode, Tylenchulus semipenetrans (23). Cadusafos is
but have not been shown to be carcinogens. commercially available in granular and microencapsu-
lated formulations.
Aldoxycarb
Fosthiazate
Aldicarb is oxidized in soils to aldicarb sulfone, which
is available in some parts of the world as the insec- Fosthiazate is a somewhat recently developed (1992) sys-
ticide/nematicide aldoxycarb. A flowable formulation is temic organophosphorus nematicide with broad-spectrum
available. activity (24). A clay-based microgranule formulation is
available. Fosthiazate provided control of the lesion
Carbofuran nematode Pratylenchus penetrans on potato (25) and
Carbofuran is another systemic insecticidal/nematicidal root knot nematodes (Meloidogyne spp.) on tobacco (26)
carbamate available in granular and liquid formulations. and M. arenaria on peanut (27), but it failed to control
Because use of carbofuran granules was associated M. javanica on tobacco and Rotylenchulus reniformis on
with bird kills, the U.S. Environmental Protection pineapple as well as fumigation with 1,3-D (28,29). It is
Agency (EPA) prohibited the use of carbofuran granules not registered for U.S. usage.
in 1994.
Other Organophosphates
Oxamyl Terbufos is a less widely used organophosphate with
Like carbofuran, oxamyl is a carbamate that is man- insecticidal and a few nematicidal uses. It is available
ufactured in liquid and granular form, but the latter in granular formulations. Fensulfothion is a systemic
is no longer registered in the United States because of previously but not currently registered for insecticidal
concerns about its consumption by birds. Oxamyl is the and nematicidal activity in the United States. Granular
only nematicide with downward-moving systemic activity and emulsifiable concentrate formulations were available.
and thus has registered foliar nematicidal applications; Phorate is primarily used as a soil insecticide but has
foliar applications did reduce Pratylenchus penetrans on nematicidal uses. Its current U.S. reregistration process
 NEMATICIDES 1107

involves the use of several risk mitigation measures. Fumigants

Organophosphate nematicides with limited worldwide use
A primary effect of halogenated hydrocarbons is to serve
but not registered in the United States include thionazin,
as alkylating agents. The sulfhydryl groups of proteins,
fosthietan, and isazofos.
in particular, are labile to methyl bromide–induced
methylation (41). With respect to research performed with
BIOCHEMICALS nematodes, EDB alkylated proteins and oxidized Fe+2
centers in the cytochrome-mediated electron transport
DiTera chain, thereby blocking respiration (40). The mode of
action of methyl isothiocyanate generators in nematodes
The nematode-parasitic fungus Myrothecium verrucaria is even more poorly understood (42); amino and hydroxyl
produces a mixture of compounds registered in 1996 as groups have been speculated as sites of attack (40).
a biologically based nematicide named DiTera. Toxicity Beyond a minimal threshold lethal concentration of a
apparently results from the synergistic action of low- fumigant, the susceptibility of a nematode to a fumigant
molecular-weight, water-soluble compounds. DiTera is has long been known to be proportional to the product
active against many plant-parasitic nematodes but not the of the concentration of the fumigant and the duration of
free-living and mammalian-parasitic nematodes studied exposure, i.e., the concentration-time product.
thus far (30). Toxic effects observed with G. rostochiensis
include disruption of hatching, movement, and response Nonfumigants
to potato root diffusate; toxicity to M. incognita did not
involve inhibition of hatching (31,32). DiTera is available Carbamates and organophosphates are well-known
as granules, a powder, and an emulsifiable suspension. reversible inhibitors of acetylcholinesterase activity in
insects. Several nonfumigant nematicides have been
demonstrated to inhibit cholinesterase in nematodes,
ClandoSan
e.g., aldicarb, carbofuran, fenamiphos, and oxamyl in
ClandoSan is a granular product made from processed M. incognita and M. javanica (43) and Aphelenchus ave-
crab and crawfish exoskeletons. The material contains nae (44). Interestingly, although carbofuran inhibits
large amounts of chitin and urea and was registered in Meloidogyne cholinesterase approximately 10,000 times
the United States in 1998 as a nematicide. Its nematicidal higher than fenamiphos (43), the latter has greater
activity (33) is believed to result from the stimulation nematicidal activity against Meloidogyne; this discrep-
of populations of nematode-antagonistic microorganisms, ancy is correlated with a much quicker metabolism of
particularly those that produce chitinase, a major fenamiphos than carbofuran by root-knot nematodes (45).
component of nematode eggshells. Proper application is Chang and Opperman (46) discovered five molecular forms
necessary to avoid phytotoxicity (33). of acetylcholinesterase in M. arenaria and M. incognita;
the forms could be divided into three classes, one of which
was highly resistant to aldicarb and fenamiphos.
Sincocin
Given that nonfumigant nematicides inhibit nematode
Sincocin is the trade name of the mixture registered acetylcholinesterase, it is not surprising that many of
in 1997 as ‘‘Plant Extract 620’’ with the U.S. EPA. the symptoms induced in nematodes reflect nervous
It consists of a blend of extracts from the prickly system dysfunction. These symptoms include stylet
pear Opuntia lindheimeri, the oak Quercus falcata, the thrusting, twitching, trembling, convulsions, soiling and
sumac Rhus aromatica, and the mangrove Rhizophora uncoiling, other uncoordinated movements, inhibited
mangle. Sincocin has provided control of the citrus penetration, and eventual paralysis if the concentration
nematode on orange roots (34), the reniform nematode is sufficiently high (39,47,48). Nematode recovery from
on sunflower (35), and the sugarbeet cyst nematode (36); acetylcholinesterase inhibitor treatment can occur within
but control of M. incognita on cassava and R. similis on a short time, even for the case of the stem and bulb
anthurium was less successful than that provided by other nematode, Ditylenchus dipsaci, exposed to 10-mg/ml
methods (37,38). Its mode of action has not been fully oxamyl for a day (48). In some cases, however, recovery
elucidated. may not occur, as with A. avenae exposed to fenamiphos,
but not carbofuran (49). The speed of recovery from
acetylcholinesterase inhibition varies among inhibitors,
MODE OF ACTION and nematodes that grossly appear fully recovered still
can exhibit pronounced acetylcholinesterase inhibition in
In general, nematode developmental stages that are enzyme assays.
active are more susceptible to nematicides than are rest- Because contact nematicide concentration in agricul-
ing stages (12,39). The detailed 20-year-old review by tural soils following application is usually not sufficiently
Wright (40) on nematicidal mode of action remains rel- high to kill nematodes, the primary organismal mode of
evant because few new nematicides have been introduced action may be temporary paralysis, interference with host
since its publication. Moreover, the broad-spectrum activ- finding, inhibition of hatching, or disruption of some other
ity of most nematicides has resulted in much of their process (10). For example, the three carbamates aldicarb,
basic biochemical effects being documented in insects or carbofuran, and cloethocarb inhibited H. schachtii juve-
mammals instead of nematodes. nile mobility at concentrations of nematicide that occur in
1108 NEMATICIDES

field situations, whereas inhibition of hatching occurred In another investigation, the free-living nematode
at concentrations not likely to occur in the field (50). Rhabditis oxycerca was bred for 400 generations in order
Because soil is a heterogeneous mixture, complete to obtain strains adapted to reproducing on concentrations
eradication of a nematode population with a chemical of 600- and 480-µg/ml aldicarb and oxamyl, respectively.
nematicide, even a fumigant, is an unlikely achievement. Compared with wild type, the two mutant strains were
Moreover, contact nematicides are used at levels insuffi- characterized by decreased size (particularly in the tail
cient to induce immediate death. Nonetheless, the inhibi- region), tolerance of warm temperature, production of
tion of movement and penetration is usually substantial offspring, and migration in electric fields, among other
enough to result in lack of economic damage. Sometimes characteristics. In nematicide solutions, the wild type
the reduction in nematode populations is not sufficiently exhibited decreased motility, electric field migration, and
long to eliminate the need for postplant reapplication of reproduction (53).
nematicides, however, especially for perennials or crops In a third study, genetically selected strains of the
with long growing seasons. Nonetheless, higher initial insect pathogen Heterorhabditis bacteriophora possessed
nematicide application rates are often not cost-effective 8–70-fold increased resistance to fenamiphos, avermectin,
and may be associated with increased environmental or and oxamyl (54). The enhanced resistance was generally
other risks. stable in the absence of further nematicide pressure; the
The metabolism of nematicides by nematodes has strains have obvious potential utility in integrated pest
not been extensively studied. In one interesting management systems.
investigation of the metabolism of carbofuran and
fenamiphos by root-knot nematodes, detected metabo-
lites included 3-hydroxycarbofuran, 3-ketocarbofuran, APPLICATION METHODS
fenamiphos sulfoxide, and various unidentified water-
soluble products (45). The methods for treating agricultural soils with nemati-
cides are similar to those used for other pesticides exam-
Mammalian Anthelmintics ined in this volume. Nematicide application research is
Although the purpose of this review is not to focus being driven by the need to maximize efficacy while mini-
on nematicides of veterinary or human medical impor- mizing groundwater and atmospheric contamination.
tance, the modes of action of these compounds have
been reviewed (4) and are relevant. Representatives of Fumigation
the most popular classes of compounds include the fol-
lowing: 1) nicotinic agonists such as the imidazothia- Soil fumigation requires prior preparation to be effec-
zole levamisole, the tetrahydropyrimidines pyrantel and tive (55). Prior to fumigant or nonfumigant application,
morantel, and the pyrimidine methyridine, which act as soil is often turned or tilled to increase porosity and uni-
agonists on muscle acetylcholine receptors and induce formity and promote decomposition of residual plant roots,
paralysis; 2) the GABA agonist piperazine, which induces which can serve as hiding places for nematodes or inter-
muscular paralysis, particularly in large nematodes in fere with fumigant movement. Adequate but not excessive
oxygen-poor environments; 3) macrocyclic lactones such soil moisture is critically important to the success of some
as avermectins and milbemycins, with mode of action as fumigants. Fumigants are typically injected with chisels
discussed in this review; 4) benzimidazoles such as thi- or shanks into the upper 15–40 cm of soil, with the actual
abendazole and mebendazole, which bind to β-tubulin depth a function of compound, soil structure, and crop.
and interfere with nematode microtubule formation; and Although deep injection is often required to minimize the
5) diethylcarbamazine, which appears to interfere with escape of fumigant into the surrounding air, inadequate
host and possibly nematode arachidonic acid metabolism. levels of nematicide in the upper soil layers may result in
some situations. Following fumigation, the soil surface is
RESISTANCE TO NEMATICIDES often compacted in order to retard fumigant loss from the
soil surface.
Resistance of field populations to nematicides has not The design of injection equipment modified for mini-
been well characterized and is remarkably insignificant mization of fumigant escape into the surrounding air is an
in comparison to the levels of resistance observed with active research area (56). Because the shallow chisel traces
mammalian parasites. Indeed, a recent National Academy left in treated soils provide a means for fumigant to escape
of Sciences monograph stated, ‘‘Resistance of nematodes into the atmosphere, some nematicide labels mandate
to soil fumigants has yet to be observed but systemic that the traces be covered with soil. Experimental chisels
nematocides are relatively new and it is probably only a angled to the side 45◦ in order to eliminate chisel trace
matter of time until resistance does appear’’ (51). formation have provided control of root-knot nematodes
In one interesting study, Moens and Hendrickx (52) on tomato equivalent to conventional chisels (57). Another
evaluated populations of Meloidogyne naasi, G. rosto- example of minimizing atmospheric loss is through use of
chiensis, and Pratylenchus crenatus exposed to aldicarb for single chisel injections for crops traditionally fumigated
15 years. Although some developmental differences were with dual chisels (58).
noticed between treated and control populations when Fumigation usually involves the use of plastic
challenged with aldicarb, the differences were species tarpaulins to minimize atmospheric losses and deliver
specific and were concluded to be not significant. nematicide to the target organism. Sometimes, tarpaulins
 NEMATICIDES 1109

must be in place for 10 days. Even when plastic sheeting is damage. In-furrow application sometimes is practiced but
employed, fumigant losses can exceed 50% and approach may result in lack of delivery to the root zone; in other
80% under extreme conditions (55,59). A variety of injec- cases, in-furrow application may be preferable. In some
tion temperatures and plastic sheeting compositions have cases, sidedress applications of nematicides are useful
been employed to maximize nematicidal activity and replacements or additions to at-plant applications.
reduce atmospheric losses of methyl bromide and other In other cases, broadcast application of granules or
fumigants. Impervious sheeting, warm temperatures, and sprays followed by a thorough mixing of the soil may be
deep injection often enhance nematicidal activity and per- effective. Tillage is necessary to distribute nematicide to a
mit the use of much smaller quantities of fumigant (41,59). broad enough area to provide control, and a thorough
A recovery system involving a double layer of polyethylene mixing is particularly important for nematicides with
sheeting through which air is blown to a methyl bromide poor soil mobility characteristics. Use of broadcast sprays
collection unit has reduced methyl bromide emissions in instead of granules often promotes greater uniformity
a laboratory setting (60). Buffer zones around fumigated in distribution. For many annual crops, incorporating
areas are often required to reduce the exposure of the nematicides into the upper 10–15 cm of soil provides
general population to airborne fumigants. the best balance of efficacy, expense, ease, and safety to
wildlife. Research on the distribution of granules to soils by
Irrigation various types of tillage equipment can be facilitated via the
use of sepiolite granules containing a fluorescent dye (66).
Liquid and emulsifiable formulations of nematicides can Nematodes are usually distributed unevenly in a given
often be applied through surface or drip irrigation systems. field; nematicide treatment deposits expensive chemical
The goal of delivering sufficient nematotoxic materials throughout a grower’s field, even in areas where it may
without excessive leaching is researchable but sometimes not be needed. In one interesting study, Baird et al. (67)
difficult to achieve (61). Drip irrigation in particular offers quantified the numbers of root-knot nematode juveniles
a means of precisely controlling the amount of active at specific locations in experimental cotton fields treated
ingredient delivered to a field, as well as regulating the with variable rates of aldicarb or 1,3-D applied with
amount of water, so that leaching of active ingredient prototype equipment designed to apply nematicide at
beyond the root zone and into groundwater can be rates dependent on initial nematode population levels.
eliminated. Drip irrigation also is useful for postplant Although final nematode population levels did not vary
applications, and it avoids the use of granular materials among treatments, the variable rate applications of 1,3-D
that may pose risks to birds. Use of drip irrigation also (but not aldicarb) resulted in yield increases and lowered
reduces the amount of personal protective equipment nematicide costs that justified the additional costs of
required for field workers. A substantial percentage of nematode sampling and enumeration.
pineapple production in Hawaii is drip irrigated, and drip
irrigation with ethoprop, fenamiphos, or soluble liquid Seed Dressing and Bare Root Dip
formulations of 1,3-D have been used to provide control
The reasons why few nematicides have been registered
of nematodes in pineapple production in Hawaii (61). In
as seed coatings include the difficulty in applying a
order to minimize leaching of nematicides below the root
sufficient quantity of nematicide needed to provide
zone and maximize effectiveness, fields are not irrigated
control beyond the seedling stage, the expense of
for 2 weeks following application. Successful control of
registration relative to market size, and the attraction of
P. penetrans on lilies was provided with drip-irrigated
such products to wildlife (65). Nonetheless, experimental
ethoprop, fenamiphos, sodium tetrathiocarbonate, 1,3-D,
formulations have provided some successes, as with
and oxamyl (20); similarly, drip-irrigated emulsifiable
control of P. penetrans on corn by seed treatment with
1,3-D provided control of the citrus nematode, Tylenchulus
oxamyl (68). In addition, seed-transmitted nematodes can
semipenetrans (62).
be successfully treated with nematicidal treatment of
Although less precise than drip irrigation in delivering
seeds (69). Much experimental research with biocontrol
nematicide to targeted areas, overhead spray irrigation
organisms or nematicidal natural products is performed
can also effectively convey nematicides (63). However,
with seed formulations.
injection of metam sodium into a center pivot irrigation
The principle behind bare root dips is similar to that
system was associated with higher airborne concentra-
for seed dressings; i.e., sufficient nematicide is applied
tions of MITC than that which occurred in fields receiving
to transplants to protect them at a highly vulnerable
metam sodium at depths of 5, 15, and 25 cm (64).
time. Root dips have provided nematode control in several
situations (8).
Granules and Broadcast Sprays
The most widely practiced method of applying nonfumi- NEMATICIDE ECOLOGY
gant nematicides is with granular formulations. Methods
for application of nonfumigants to soil have been thor- Effects of Temperature on Activity
oughly reviewed (65). In some cases, adequate control can The effects of temperature on nematicide efficacy are
be achieved by band application of nematicides at or before complex and not well studied. Increases in temperature
sowing. In band application, plant roots may eventually may stimulate the metabolic activity of the target
grow beyond the treated area at a time when the root nematode, alter the solubility of the chemical in the
system will be sufficiently vigorous to not suffer serious aqueous or vapor phases, and alter the rate of microbial
1110 NEMATICIDES

or chemical destruction of the nematicide. Because capable of oxidizing methyl bromide to form formaldehyde
nematicides are often applied at the beginning of a growing and inorganic bromide (77).
season, low soil temperature may be of concern with Aldicarb and fenamiphos are initially degraded in soils
respect to efficacy in some cases (70). The activity of into sulfone and sulfoxide derivatives with target and
EDB and 1,3-D against the motility and infectivity of nontarget toxicity and with enhanced mobility correlated
M. javanica in fumigation chambers was much less at 5 ◦ C with increased solubility in water (73,79). Transformation
than at 15 ◦ C (12). Similarly, methyl bromide exhibited of fenamiphos sulfoxide into sulfone progresses much
greater activity against the dagger nematode Xiphinema more rapidly in subsurface soils than in surface soils (80).
index and M. incognita at 30 ◦ C than at 15 ◦ C in soils Aldicarb and fenamiphos sulfoxides may be the major
in sealed cans (71). The enhancement of methyl bromide active materials (73,81). Aldicarb is further degraded into
and 1,3-D activity against Tylenchulus semipenetrans by oximes and nitriles. The sulfoxide and sulfone derivatives
high temperature in controlled-temperature experiments of fenamiphos and aldicarb are more mobile in soils
indicated that nematicide efficacy could possibly be than are the parent nematicides and have the potential
improved by soil solarization (72). to more readily contaminate groundwater (82). Unlike
aldicarb, the carbamate group is hydrolyzed in oxamyl.
Effects of Soil Structure on Activity The degradation of oxamyl into nontoxic oximes at 10
The physicochemical composition of soil is a critical factor different sites was generally associated with increased
influencing nematicidal efficacy. Nematicides diffuse pH, temperature, and moisture (83).
more slowly through soils with small pore spaces, fine Microbial transformation of nematicides is an impor-
particle size, and low moisture content (73). A high tant factor affecting efficacy. As with other types of pesti-
clay content can result in increased adsorption and cides, repeated application of nematicides to agricultural
poorer movement of nematicide (47,61,74). Nematicide soils can result in enhanced microbial degradation and
adsorption onto organic matter is strongly correlated decreased efficacy (77). For example, decreased efficacies of
with lipophilicity (10); organic matter can reduce efficacy, aldicarb, ethoprop, and oxamyl against potato cyst nema-
either by increasing moisture content, by acting as an todes following multiple applications were associated with
adsorbent, by providing receptors for alkylating agents, increased transformation of the nematicides (75). When
or by increasing microbial populations that are capable previously treated soils were autoclaved, these effects
of degrading the applied nematicide (75). The movement did not occur. Similar phenomena have been observed
of contact nematicides away from their application zone in fenamiphos-treated soils; the amount of time required
is similarly a function of adsorption onto organic matter. for enhanced degradation to disappear has been reported
Fumigants, ethoprop, and fenamiphos are less effective in as being from 1 to 5 or more years, depending on the
soils with large amounts of organic matter, but aldicarb study (79,84,85). Enhanced biological degradation of 1,3-D
and oxamyl are effective in soils with a wide range or methyl isothiocyanate has been described in a num-
of organic matter concentrations (65). Riegel et al. (76) ber of soils, and various bacteria capable of mineralizing
noted that 1,3-D applied to microplots supplemented with 1,3-D have been isolated (77,86,87). In at least some of
yard waste compost was less effective in suppressing these bacteria, a haloalkane dehalogenase gene carried
M. incognita reproduction on tomato than in control on a plasmid is involved in enhanced degradation (86,87).
microplots. Adsorption onto soil organic matter, although One such organism (Pseudomonas cichorii) can grow on
undesirable from the perspective of nematicide efficacy, low concentrations of 1,3-D as its sole carbon and energy
may be negatively correlated with tendency to contaminate source (88).
groundwater. Enhanced microbial degradation of nematicides is
a somewhat unpredictable phenomenon, has not been
Degradation of Nematicides reported with some nematicides, and is generally
unpredictable in occurrence (75,77,89). When accelerated
Once applied to soils, any pesticide is subject to biological
transformation exists, the responsible microorganisms
and physicochemical transformations. Transformation
generally transform compounds chemically related to
products may have less or greater toxicity than the parent
the original nematicide (75). Exceptions occur when the
compound. An analysis of various values reported in the
enhanced biodegradation occurs as a result of metabolism
literature indicated half-lives of parent compounds of
of a specific part of the nematicide, such as occurred in
2–190 days, depending on the parent compound and the
a situation when enhanced ethoprop degradation resulted
physicochemical properties of the soil (75). Nordmeyer (10)
from increased hydrolysis of the P−S bond in the S-propyl
regarded a 14-day half-life as ideal for a balance between
moiety of ethoprop (90). In this case, two strains of Pseu-
efficacy and environmental safety.
domonas putida capable of rapidly degrading ethoprop
In soils, 1,3-D is first biologically or chemically
were isolated from the soil (91).
hydrolyzed to 3-chloroallyl alcohol, which is then oxi-
dized to chloroacrylic acid, which in turn is converted
Effects on Nontarget Organisms
to simple short-chain organic acids (77). Chloroallyl alco-
hol and chloroacrylic acid also are toxic to humans and are The nontarget effects of nematicide applications are
of regulatory concern (78). The primary route of chemical reviewed in this volume and elsewhere; a detailed
degradation of methyl bromide in soil is through hydrolysis evaluation is beyond the scope of this review. Because
to yield methanol and bromide ions and through methy- of their broad-spectrum activities, most nematicides
lation. Some bacteria, particularly nitrifying bacteria, are radically alter soil flora and fauna. Fumigant usage
 NEMATICIDES 1111

may result in the absence of nematode competitors, sector researchers in pursuing the development of new
predators, and parasites in soils (92). The elimination chemical nematicides. In some countries, demand for
of mycorrhizae by methyl bromide can result in poorer nematicides is high. Although the nematicide market
plant growth (55). Long-term aldicarb treatment of potato in the United States represents a small fraction of
fields decreased the number of bacterial genera and total pesticide usage, in The Netherlands, nematicides
species, decreased the population levels of plant growth- represent more than 60% of the total pesticides used in
promoting rhizobacteria, and increased total bacterial agriculture (13).
biomass compared to untreated soils (93). Future control of nematodes will increasingly rely
Nematicides can greatly alter the subsequent structure on site-specific, sustainable management practices, as
of nematode communities in soils; for example, Praty- well as on integrated pest management involving the
lenchus recolonized methyl bromide–treated pasture soil, judicious use of nematicides. Nonchemical strategies
replacing Helicotylenchus as the dominant phytoparasitic available to growers for some nematode-host combi-
nematode (94). Nematodes and other organisms play a nations include crop rotation, altered planting time,
complex role in agroecosystems (7); use of broad-spectrum resistant germplasm, solarization, fallow, and nematode-
biocides makes it difficult to exploit some of these roles. suppressive soil amendments. Many of these strategies
are less expensive and sometimes less effective than is
Environmental Contamination traditional chemical control.
The development of new nematicides has been
One of the greater environmental problems sometimes reviewed (8,10,99). Prospective compounds can originate
associated with nematicide usage is groundwater contam- from empirical screening or by rational design of com-
ination. Indeed, the initial detection of the nematicides pounds that can exploit biological or biochemical weak-
DBCP and aldicarb in groundwater in the United States nesses of nematodes. The underlying biochemistry of
over 20 years ago led to the stimulation of scientific and plants and nematodes is similar in many respects; suc-
regulatory interest in pesticide contamination of ground- cessful transfer of a rationally designed compound from
water that continues to this day (95). Even though DBCP laboratory to the field has not yet been achieved, in no
usage was prohibited in 1977, groundwater contamina- small part because of the previously described difficulties
tion persists (96). In 1990, the manufacturer of Temik in nematicide design.
(aldicarb) announced a voluntary halt on its sale for use It is beyond the scope of this review to list every com-
on potatoes because of concerns about groundwater con- pound described as possessing nematotoxicity. However,
tamination. The following year, a train wreck released the following compounds are worthy of discussion. Biora-
72,000 L of metam sodium into the Upper Sacramento tionals are listed at the conclusion.
River and resulted in soil microbial changes that per-
sisted for at least a year (97). When the special review of Methyl Iodide and Propargyl Bromide
1,3-D by the U.S. EPA was terminated, several measures
The immediate demand for methyl bromide replacements
for reducing potential groundwater contamination were
makes it likely that the next nematicides to be registered
instituted, such as prohibition of usage within 100 feet
could be compounds similar to methyl bromide; for
of drinking-water wells, in areas overlying karst geology,
example, methyl iodide and propargyl bromide. The
and in several states with certain soil types and where
latter has provided experimental control of M. incognita
groundwater is 50 feet from the soil surface (78).
on tomato, although the explosiveness of the compound
As previously indicated, 1,3-D use was suspended in
requires that innovative formulations be developed (100).
California in 1990 for several years because of its detection
Methyl iodide exhibits greater toxicity to phytoparasitic
in air distant from application sites, specifically in a school.
nematodes than does methyl bromide, perhaps because
This has resulted in the creation of 300-foot–wide buffer
of greater reactivity or lower volatility than methyl
zones around residences for fumigation (100 feet wide if
bromide (101), and it is degraded in the atmosphere before
fields are drip irrigated). In addition, ‘‘township caps’’ limit
it has the opportunity to react with ozone (102). Because it
the total amount of 1,3-D that can be used in a given area
is a liquid at ambient temperature, methyl iodide is easier
in California (98).
than methyl bromide to apply safely. Methyl iodide has
provided control of M. incognita on carrot (102), but it also
THE FUTURE eliminated Rhizobium nodules (101).

Presently, only a few chemical nematicides remain, and DMDP

some of these will undoubtedly be withdrawn before the One compound moving closer to agricultural utilization
end of the decade, if not before the end of this year. is 2,5-dihydroxymethyl-3,4-dihydroxypyrrolidine (DMDP),
The economic cost of research and registration of new a naturally occurring sugar analog from the tropical
chemicals is an enormous hurdle for a new chemical legume Lonchocarpus felipei, which inhibited hatching
nematicide to overcome. Of the 497 new active ingredients of G. pallida and movement of G. rostochiensis (103). The
registered for use as pesticides from 1967 to 1997, only compound is downwardly mobile in plant phloem; foliar
seven were registered as nematicides (11). Nonetheless, applications on tomato decreased galling induced by
the decreasing number of compounds and the enormous M. incognita. Use as a nematicide has been patented,
economic damage caused by phytoparasitic nematodes and plans are underway to produce this compound from
continues to maintain the interest of private and public natural sources in tropical America.
1112 NEMATICIDES

Avermectins of SAR inducers such as salicylic acid and benzo-(1,2,3)-

thiadiazole-7-carbothioic acid S-methyl ester as nematode
The avermectins are often drugs of choice for treatment
control agents (111–113).
of human and veterinary nematode infections. These
macrocyclic lactones have experimentally provided suc-
cessful control of nematodes in the field (104,105) but are Hatching Stimulants and Inhibitors
not registered for use against phytoparasitic nematodes. Although not nematicidal, hatching stimulants could be
Meloidogyne javanica and R. similis on banana were con- used to induce hatch in the absence of host plants, result-
trolled by injections of abamectin into the pseudostem ing in the death of host-deprived nematodes. Stimulation
as well as preplant applications of fenamiphos (106). The of potato cyst nematode hatching by potato root diffusate
effects of avermectin have been best documented in the has been investigated for decades and results from a com-
mammalian intestinal parasite Ascaris and the free-living plex mixture of at least 20 distinct compounds (114). A
nematode Caenorhabditis elegans. Avermectin paralyzes hatching stimulant for the soybean cyst nematode was
somatic musculature in Ascaris and pharyngeal muscula- isolated from 1058 kg of dried kidney bean roots and
ture in C. elegans by irreversibly opening glutamine-gated identified as a complex triterpenoid derivative named
chloride channels (5,107). glycinoeclepin A (115). Two simpler analogs stimulated
hatch, although at higher concentrations than required
Sodium Azide than for glycinoeclepin A (116). Two other simpler analogs
Sodium azide is a potent inhibitor of cytochrome oxidase were also synthesized (117); one inhibited hatch but the
and disrupts the respiratory electron transport chain. It other stimulated it.
was registered as a nematicide in the United States in
1974, but its nematicidal use was withdrawn. Preplant Transgenic Proteins
applications provided successful control of M. incognita
and Helicotylenchus dihystera on potato (108). Interest in As with most other classes of plant pests and pathogens,
this compound is intensifying because of the urgent need transgenically based plant resistance is expected by
for methyl bromide replacements. many to provide the basis for future management
of phytoparasitic nematodes. Although no transgenic
Furfural system has resulted in commercial success equivalent
to that of insect-resistant plants expressing Bacillus
Like sodium azide, furfural is being investigated as a thuringiensis toxins, substantial progress is being made.
replacement for methyl bromide. Furfural has provided For example, transgenic plants expressing a proteinase
control of nematodes on pineapple and cotton (109,110). inhibitor resulted in a 50% decrease in the reproduction of
M. incognita, compared to control rice plants (118). Strains
Phytochemicals of B. thuringiensis are known that produce toxins to the
Several researchers are attempting to develop phyto- free-living nematode Caenorhabditis elegans (119).
chemical-based strategies for nematode control (19). To
some extent, this research has its roots in the complex Behavior-Modifying Compounds
chemical interactions between plants and nematodes. In
addition, there has been a vast body of work involving A variety of behaviors are involved in host- and mate-
the application of green manures to or within soils. finding by nematodes. The only nematode compound
Moreover, because members of the plant kingdom produce with sex attractant activity is vanillic acid, which is
a variety of secondary metabolites, many investigators produced by soybean cyst nematode females. Several
have ventured beyond allelopathic interactions and looked synthetic analogs did lower cyst production in field
for nematode-antagonistic substances in plant parts and microplot experiments (120). The possibility of using
unlikely to be involved in nematode-plant interactions, specific compounds to attract nematodes to toxic baits was
such as leaves, or in algae or fungi. A rich assortment shown in laboratory experiments with T. semipenetrans,
of over 100 different secondary metabolites has been and three different nematicides whose activity was
identified as being responsible for plant- or fungal- increased by the attractant sodium acetate (121). When
mediated nematotoxicity (19). precise molecular interactions between nematodes and
In recent years, various plant-based products have their hosts important to parasitism are discovered, these
appeared with putative antinematodal activity. Most of could be exploited.
these have not been available long enough to permit
satisfactory evaluation by agricultural researchers. A Steroids and Hormones
few of these products may curtail nematode damage by
Nematodes possess a nutritional requirement for sterols;
stimulating plant growth.
dietary sterols are converted to sterols typical of nema-
todes. Several compounds interfere with the conversion of
Systemic Acquired Resistance Inducers
plant sterols to nematode sterols and disrupt the nematode
Systemic acquired resistance (SAR) is a phenomenon in life cycle (122). The identification of a nematode hormone
which exposure of plants to one pathogen or elicitor can has not been achieved, a necessary first step to permit
result in resistance to several diverse kinds of pathogens. their exploitation in a manner similar to that of insect
A few laboratories are currently investigating the use juvenile and molting hormones.
 NEMATICIDES 1113

27. N. A. Minton, T. B. Brenneman, K. Bondart, and G. W.

Acknowledgments Harrison, Peanut Sci. 20: 66–70 (1993).
Mention of trade names or commercial products in this publication 28. J. R. Rich et al., Suppl. J. Nematol. 26: 701–704 (1994).
is solely for the purpose of providing specific information and
does not imply recommendation or endorsement by the U.S. 29. B. S. Sipes, Fruits 51: 173–177 (1996).
Department of Agriculture. 30. P. Warrior et al., Pestic. Sci. 55: 376–379 (1999).
31. U. Twomey, P. Warrior, B. R. Kerry, and R. N. Perry, Nema-
BIBLIOGRAPHY tology 2: 355–362 (2000).
32. R. N. Perry, U. Twomey, R. N. Rolfe, and P. Warrior,
1. N. A. Cobb, U.S. Department of Agriculture Yearbook, 1914, Aspects Appl. Biol. 59: 53–58 (2000).
pp. 457–490. 33. T. D’Addabbo, Nematol. Medit. 23: 299–305 (1995).
2. W. B. Thomas, Suppl. J. Nematol. 28: 586–590 (1996). 34. G. Y. Osman and F. M. Salem, Anz. Schädlingskde. Pflan-
3. W. C. Campbell, J. Parasitol. 72: 45–61 (1986). zenschutz Unweltschutz 68: 179–181 (1995).

4. R. J. Martin, Parasitology 114: S111–S124 (1997). 35. A. A. Farahat, A. A. Osman, H. I. El-Nagar, and H. H.
Hendy, Bull. Fac. Agric. Univ. Cairo 44: 191–204 (1993).
5. P. Köhler, Int. J. Parasitol. 31: 336–345 (2001).
36. H. Banaszak and M. Jagusz, Prog. Plant Prot. 39: 154–159
6. J. N. Sasser and D. W. Freckman, in J. A. Veech and (1999).
D. W. Dickson, eds., Vistas in Nematology, Society of
Nematologists, Hyattsville, MD, 1987, pp. 7–14. 37. Medina, R. Crozzoli, and D. Rivas, Fitopatol. Venez. 5: 26–29
(1992).
7. K. R. Barker and S. R. Koenning, Annu. Rev. Phytopathol.
36: 165–205 (1998). 38. B. S. Sipes and K. M. Delate, Nematropica 26: 171–175
(1996).
8. N. G. M. Hague and S. R. Gowen, in R. H. Brown and
B. R. Kerry, eds., Principles and Practice of Nematode 39. A. A. F. Evans, Ann. Appl. Biol. 75: 469–473 (1973).
Control in Crops, Academic Press, Sydney, Australia, 1987, 40. D. J. Wright, in B. M. Zuckerman and R. A. Rohde, eds.,
pp. 131–178. Plant Parasitic Nematodes, Vol. III, Academic Press, New
9. R. A. Sikora and J. Hartwig, Rev. Nématol. 24: 531–536 York, 1981, pp. 421–449.
(1991). 41. O. C. Macdonald and C. Reichmuth, in C. H. Bell, N. Price,
10. D. Nordmeyer, in F. J. Gommers and P. W. T. Maas, eds., and B. Chakrabarti, eds., The Methyl Bromide Issue, Wiley,
Nematology: From Molecule to Ecosystem, European Society Chichester, U.K., 1996, pp. 150–189.
of Nematologists, Invergowrie, Scotland, 1992, pp. 281–293. 42. B. S. Sipes and D. P. Schmitt, in K. R. Barker, G. A. Peder-
11. A. L. Aspelin and A. H. Grube, Pesticides Industry Sales son, and G. L. Windham, eds., Plant and Nematode Inter-
and Usage, 1996 and 1997, U.S. Environmental Protection actions, American Society of Agronomy, Madison, WI, 1998,
Agency, Publication 733–R-99-001, 1999. pp. 173–185.
12. M. V. McKenry and I. J. Thomason, Hilgardia 42: 422–438 43. D. Nordmeyer and D. W. Dickson, Rev. Nématol. 23: 311–
(1974). 316 (1990).
13. C. H. Schomaker and T. H. Been, Nematology 1: 19–29 44. D. J. Pree, J. L. Townshend, and D. E. Archibald, J. Nema-
(1999). tol. 19: 188–193 (1987).
14. L. A. Thrupp, Int. J. Health Serv. 21: 731–757 (1991). 45. D. Nordmeyer, D. W. Dickson, L. T. Ou, and H. L. Cromroy,
Pestic. Biochem. Physiol. 34: 179–184 (1989).
15. D. E. Munnecke and S. D. Van Gundy, Annu. Rev. Phy-
topathol. 17: 405–429 (1979). 46. S. Chang and C. H. Opperman, Mol. Biochem. Parasitol. 49:
16. A. S. Csinos et al., Crop Prot. 19: 39–49 (2000). 205–214 (1991).

17. S. J. Locascio et al., HortScience 32: 1208–1211 (1997). 47. A. G. Whitehead, Ann. Appl. Biol. 75: 439–453 (1973).

18. E. M. Smedley, J. Helminthol. 17: 31–38 (1939). 48. C. H. Opperman, in F. J. Gommers and P. W. T. Maas, eds.,
Nematology: From Molecule to Ecosystem, European Society
19. D. J. Chitwood, Annu. Rev. Phytopathol. 40: 221–249 (2002). of Nematologists, Invergowrie, Scotland, 1992, pp. 60–72.
20. B. B. Westerdahl et al., Suppl. J. Nematol. 25: 758–767 49. D. J. Pree, J. L. Townshend, and K. J. Cole, J. Nematol. 22:
(1993). 182–186 (1990).
21. F. A. Norris, E. G. Jordan, and A. Guardigli, Anal. Meth. 50. J. Hartwig and R. A. Sikora, Rev. Nématol. 14: 525–530
Pestic. Plant Growth Regulators 16: 3–20 (1988). (1991).
22. P. Quénéherve, T. Mateille, and P. Topart, Rev. Nématol. 51. M. Berenbaum, Committee on the Future Role of Pesticides,
14: 221–229 (1991). National Academy of Sciences, The Future Role of Pesticides
23. M. A. McClure and M. E. Schmitt, Suppl. J. Nematol. 28: in U.S. Agriculture, National Academy Press, Washington,
624–628 (1996). D.C., 2000, p. 48.
24. T. Koyanagi, O. Imai, and K. Yoshida, J. Pestic. Sci. 23: 52. M. Moens and G. Hendrickx, Fund. Appl. Nematol. 21:
174–183 (1998). 199–204 (1998).
25. J. Kimpinski, Suppl. J. Nematol. 29: 685–689 (1997). 53. L. Kämpfe and H. Schütz, Nematologica 41: 449–467 (1995).
26. M. P. Pullen and B. A. Fortnum, Suppl. J. Nematol. 31: 54. I. Glazer, L. Salame, and D. Segal, Biocontrol Sci. Technol.
694–699 (1999). 7: 499–512 (1997).
1114 NEMATICIDES

55. L. Klein, in C. H. Bell, N. Price, and B. Chakrabarti, eds., 85. J. H. Smelt, A. E. van de Peppel-Groen, L. J. T. van der Pas,
The Methyl Bromide Issue, Wiley, Chichester, U.K., 1996, and A. Dijksterhuis, Soil Biol. Biochem. 28: 1757–1765
pp. 191–235. (1996).
56. Anonymous, Methyl Bromide Alternatives, Vol. 7, USDA, 86. C. Verhagen, E. Smit, D. B. Janssen, and J. D. van Elsas,
Washington, D.C., 2000, pp. 5–6. Soil Biol. Biochem. 27: 1547–1557 (1995)
57. C. Riegel et al., Nematropica 31: 291–295 (2001). 87. C. Verhagen, G. Lebbink, and J. Bloem, Soil. Biol. Biochem.
28: 1753–1756 (1996).
58. R. C. Schneider et al., Pestic. Sci. 30: 243–257 (1990).
88. G. J. Poelarends et al., Appl. Environ. Microbiol. 64: 2931–
59. D. Wang et al., Environ. Sci. Technol. 31: 3017–3022 (1997).
2936 (1998).
60. D. E. Chitwood and M. A. Deshusses, Environ. Sci. Technol.
89. A. W. Johnson, Suppl. J. Nematol. 30: 40–44 (1998).
35: 636–642 (2001).
90. D. G. Karpouzas and A. Walker, Pest Management Sci. 56:
61. R. C. Schneider, R. E. Green, and W. J. Apt, Acta Hort. 334:
540–548 (2000).
351–360 (1993).
91. D. G. Karpouzas and A. Walker, J. Appl. Microbiol. 89:
62. D. Wang and S. R. Yates, Pestic. Sci. 55: 154–160 (1999).
40–48 (2000).
63. A. W. Johnson, Suppl. J. Nematol. 26: 697–700 (1994).
92. B. S. Sipes and D. P. Schmitt, Suppl. J. Nematol. 27:
64. I. A. M. Saeed, D. I. Rouse, and J. M. Harkin, Pest Manag. 639–644 (1995).
Sci. 56: 813–817 (2000).
93. A. V. Sturz and J. Kimpinski, Plant Pathol. 48: 26–32
65. A. G. Whitehead, Brit. Crop Prot. Counc. Monograph 39: (1999).
309–317 (1988).
94. G. W. Yeates and H. van der Meulen, Biol. Fert. Soils 21:
66. S. Woods et al., Soil Tillage Res. 51: 17–23 (1999). 1–6 (1996).
67. R. E. Baird, J. R. Rich, and D. Waters, Nematol. Medit. 29: 95. S. Z. Cohen, J. Environ. Sci. Health B31: 345–352 (1996).
247–254 (2001). 96. L. A. Soutter and K. Loague, J. Environ. Qual. 29: 1794–
68. M. Chiba, G. J. Fulop, B. D. McGarvey, and J. W. Potter, J. 1805 (2000).
Agric. Food Chem. 41: 2160–2163 (1993). 97. G. E. Taylor et al., Environ. Toxicol. Chem. 15: 1694–1701
69. R. Tacconi, R. Santi, and R. Gironi, Nematol. Medit. 27: (1996).
291–293 (1999). 98. J. Carpenter, L. Lynch, and T. Trout, Calif. Agric. 55(3):
70. I. G. Grove and P. P. J. Haydock, Aspects Appl. Biol. 59: 12–18 (2001).
103–108 (2000). 99. J. Feldmessr, J. Kochansky, H. Jaffe, and D. Chitwood, in
71. N. Abdalla and B. Lear, Plant Dis. Reptr. 59: 224–228 J. L. Hilton, ed., Agrochemicals of the Future, Rowman and
(1975). Allanheld, Totowa, NJ, 1985, pp. 327–344.
72. S. Xue, J. Gan, S. R. Yates, and J. O. Becker, Pest Manage- 100. J. W. Noling and J. P. Gilreath, USDA Methyl Bromide
ment Sci. 56: 737–742 (2000). Alternatives Vol. 6: 9–10 (2000).
73. R. H. Bromilow, Ann. Appl. Biol. 75: 473–479 (1973). 101. J. O. Becker et al., Pestic. Sci. 52: 58–62 (1998).
74. S. Q. Zheng et al., Sci. Total. Environ. 156: 1–9 (1994). 102. C. M. Hutchison et al., Nematology 14: 407–414 (1999).
75. J. H. Smelt and M. Leistra, in F. J. Gommers and P. W. T. 103. A. N. E. Birch et al., Nematologica 39: 521–535 (1993).
Maas, eds., Nematology: From Molecule to Ecosystem, 104. J. N. Sasser, T. L. Kirkpatrick, and R. A. Dybas, Plant Dis.
European Society of Nematologists, Invergowrie, Scotland, 66: 691–693 (1982).
1992, pp. 266–280.
105. K. Blackburn, S. R. Alm, and T. S. Yeh, Suppl. J. Nematol.
76. C. Riegel et al., J. Nematol. 33: 289–293 (2001). 28: 687–694 (1996).
77. L.-T. Ou, J. Nematol. 30: 56–64 (1998). 106. R. K. Jansson and S. Rabatin, Suppl. J. Nematol. 29: 695–
78. U.S. Environmental Protection Agency, Fed. Reg. 66: 702 (1997).
58468–58472 (2001). 107. L. Avery and J. H. Thomas, in D. L. Riddle, T. Blumenthal,
79. L.-T. Ou, Soil. Sci. Soc. Am. J. 55: 716–722 (1991). B. J. Meyer, and J. R. Preiss, eds., C. elegans II, Cold
Spring Harbor Laboratory Press, Plainview, NY, 1997,
80. R. S. Kookana, C. Phang, and L. A. G. Aylmore, Aust. J. Soil pp. 679–716.
Res. 35: 753–761 (1997).
108. R. Rodrı́guez-Kábana and P. A. Backman, Plant Dis. Reptr.
81. R. F. Davis, R. D. Wauchope, and A. W. Johnson, J. Nema- 59: 528–532 (1975).
tol. 26: 511–517 (1994).
109. B. S. Sipes, Acta Hort. 425: 457–464 (1997).
82. E. Loffredo, N. Senesi, V. A. Melilli, and F. Lamberti,
J. Environ. Sci. Health B26: 99–113 (1991). 110. E. M. Bauske et al., Nematropica 24: 143–150 (1995).

83. E. Ambrose, P. P. J. Haydock, and A. Wilcox, Aspects Appl. 111. B. Chinnasri, B. S. Sipes, and D. P. Schmitt, J. Nematol. 33:
Biol. 59: 41–51 (2000). 253 (2001).

84. J. P. E. Anderson and A. Lafuerza, in J. P. E. Anderson, 112. V. N. Kempster, K. A. Davies, and E. S. Scott, Nematology
D. J. Arnold, F. Lewis, and L. Torstensson, eds., Proc. Int. 3: 35–43 (2001).
Symp. Environ. Aspects Pestic. Microbiol, Sigtuna, Sweden, 113. B. Nandi, N. C. Sukul, and S. P. Sinha Babu, Allelopathy J.
1992, pp. 184–192. 7: 285–288 (2000).
 NITRATE IN GROUNDWATER 1115

114. K. J. Devine, J. Byrne, N. Maher, and P. W. Jones, Ann. this period. Environmental concern has centered mainly
Appl. Biol. 129: 323–334 (1996). on the formation of algal blooms and excessive growth
115. A. Fukuzawa, A. Furusaki, M. Ikura, and T. Masamune, of water plants in surface fresh waters and in the coastal
J. Chem. Soc. Chem. Commun. 1985: 222–224,748 (1985). areas of the sea. Worries about our health spring from fears
116. A. Miwa, Y. Nii, H. Okawara, and M. Sakakibara, Agric. that nitrate in potable water might cause stomach cancer
Biol. Chem. 51: 3459–3461 (1987). in adults or methemoglobinemia (‘‘blue-baby’’ syndrome)
in infants. Recent medical research, however, suggests
117. G. A. Kraus, B. Johnston, A. Kongsjahju, and G. L. Tylka,
J. Agric. Food Chem. 42: 1839–1840 (1994).
not only that nitrate is beneficial to our health but also
that we produce it within our bodies. Water supplies are
118. P. Vain et al., Theor. Appl. Genet. 96: 266–271 (1998). drawn from both ground and surface waters according to
119. J. S. Griffitts, J. L. Whitacre, D. E. Stevens, and R. V. their availability. This article is concerned with nitrate in
Aroian, Science 293: 860–864 (2001). groundwater, which has health, rather than environmen-
120. S. L. F. Meyer et al., J. Nematol. 29: 282–288 (1997). tal, implications, but environmental issues are not ignored.
121. L. W. Duncan and M. M. Abou-Setta, Nematropica 25: 173–
175 (1995). NOMENCLATURE
122. D. J. Chitwood, Crit. Rev. Biochem. Mol. Biol. 34: 273–284
(1999). ‘‘Nitrate’’ is the chemical name for the NO3 − ion, and
it is not known by any other. The practice of referring to
‘‘nitrates’’ in natural waters and water supplies is incorrect
FURTHER READING
because, as in all dilute electrolyte solutions, the anions
and cations are dissociated from each other. The species
Barker, K. A., Pederson, G. A., and Windham, G. L., eds., Plant
and Nematode Interactions, American Society of Agronomy,
with which we are concerned is, therefore, the free nitrate
Madison, WI, 1998. ion, which is unique rather than plural.
Brown, R. H. and Kerry, B. R., eds., Principles and Practice
of Nematode Control in Crops, Academic Press, Sydney, Structural Formula
Australia, 1987. The nitrate ion, NO3 − , has a symmetrical planar trigonal
Perry, R. N. and Wright, D. J., eds., The Physiology and Bio- structure in which the nitrogen atom has a formal positive
chemistry of Plant-Parasitic and Free-Living Nematodes, CAB charge. Two negative charges are shared between the
International, Wallingford, U.K., 1998.
three oxygen atoms in a resonance structure comprising
Sharma, S. B., ed., The Cyst Nematodes, Kluwer Academic three electronic conformations in which each of the oxygen
Publishers, Dordrecht, 1998.
atoms, in turn, is without charge. The uncharged atom has
Whitehead, A. G., Plant Nematode Control, CAB International, two electron pairs and is attached to the nitrogen atom by
Wallingford, UK, 1998.
a π -bond, and the charged atoms have three electron pairs.

PHYSICAL PROPERTIES
NITRATE IN GROUNDWATER
Solubility
THOMAS ADDISCOTT
Rothamsted Experimental The salts formed by the nitrate ion are generally soluble,
Station and calcium nitrate has such a high affinity for water
Harpenden, Herts, that it is deliquescent, which means that it will pick up
United Kingdom moisture from the air and dissolve in it. The main cations
in groundwater are likely to be calcium, magnesium,
potassium, sodium, iron, and aluminium, and the salts
INTRODUCTION
they form with nitrate are all very soluble (Table 1).
Ammonium nitrate is also highly soluble. Calcium is
The nitrate ion is one of the more ubiquitous chemical
usually the dominant cation in groundwater, and the
substances on the planet and is nearly always found in
nitrate concentration at the limit of solubility for calcium
water. Most of the water around us contains nitrate, but
nitrate is 32,000 times greater than the U.S. limit for
the water with which we are concerned here is ground-
nitrate concentration in potable water and 28,000 times
water, which is water accumulated in the saturated zones
greater than the E.C. limit. Solubility cannot, therefore,
of certain rock formations, usually at depth. Most of this
limit nitrate concentrations in groundwater.
water has passed through the soil before it accumulates, so
that activities at the soil surface, particularly agriculture,
Sorption
can have a strong influence on the concentrations of nitrate
and other agrochemicals in groundwater. Despite its com- Nitrate, being an anion, is attracted to positively charged
monplace nature, nitrate has for at least two decades surfaces. Nearly all agricultural soils in the developed
been a source of widespread concern because of its per- world are usually maintained at pH values that are not
ceived effects on our environment and our health. As a acid enough to permit the development of the positive
result, the ‘‘nitrate problem’’ has been a major influence charges that will retain nitrate. However, there are some
on agroecological research in the developed world during soils, particularly highly weathered soils in the Tropics,