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and Agri-Food Canada, Southern Crop Protection and Food Research Centre, P.O. Box 6000,
4902 Victoria Ave. N., Vineland Station, Ontario, Canada L0R 2E0; 2University of Guelph,
Department of Plant Agriculture, Box 587, Simcoe, Ontario, Canada N3Y 4N5.
Received 20 August 2001, accepted 20 November 2002.
Potter, J. W. and McKeown, A. W. 2003. Nematode biodiversity in Canadian agricultural soils. Can. J. Soil Sci. 83: 289302.
The biodiversity of soil-inhabiting nematodes in Canada is incompletely known, as large areas of Canadas landmass have not been
surveyed for nematode fauna. Nematodes considered as indigenous are generally well adapted to a variety of ecological niches and
climatic zones. Much of the available information is based on agricultural ecosystems and agricultural species, and thus is biased
toward conditions in disturbed ecosystems and away from primeval ecology. Introduced nematode species are frequently quite
pathogenic, even to exotic host plants from the same geographic point of origin. Estimates of crop loss due to single species infestations of pathogenic nematodes and the costs of nematode control using chemicals are reasonably well known, averaging about
10% of crop value, but ranging to 100% depending on the situation; the cost of damage by multiple-species infestations is less
defined. Nematode-suppressive mechanisms are understood in only a few plant species; sulfur appears to be important as a constituent of active compounds in suppressive plants of agricultural origin. Similarly, some native plants are equally adapted with
allelopathic chemicals that suppress nematodes. Management of nematode populations in agricultural soils by integrated crop management methods is at an early stage, requiring research to quantify effects of nematode-suppressive plants and soil amendments
containing nitrogen. An integrated program could include nematode-suppressive plants, appropriate soil amendments, and the promotion of microbial antagonists. Different mathematical methods may be required to analyze and explain multi-factor nematode
control systems. Less-toxic management systems could benefit the soil-inhabiting nematodes that predate arthropod soil pests.
Further research on soil-borne nematodes may demonstrate the value of nematodes as indicators of agroecosystem health and environmental pollutants.
Key words: Biocontrol, biodiversity, nematode distribution, nematode management, soil ecology
Potter, J. W. et McKeown, A. W. 2003. Biodiversit des nmatodes dans les sols agricoles canadiens. Can. J. Soil Sci. 83:
289302. On connat mal la biodiversit des nmatodes qui peuplent les sols canadiens, leur population nayant fait lobjet
daucun recensement sur une vaste partie du territoire national. En gnral, les nmatodes indignes sont bien adapts une gamme
de niches cologiques et de zones climatiques. Une bonne part de linformation disponible repose donc sur les cosystmes et les
espces agricoles, do lexistence dun biais vers les cosystmes perturbs plutt que lcologie primitive . Les espces
introduites sont souvent trs pathognes, mme pour les plantes htes exotiques ayant la mme origine gographique. Les pertes
agricoles attribuables linfestation par une seule espce de nmatode pathogne et le cot des produits employs pour lutter
contre les nmatodes sont raisonnablement bien connus et varient den moyenne 10 % la totalit de la valeur des cultures, selon
les circonstances; on est moins sr du cot des dommages causs par les infestations de plusieurs espces. Dautre part, on ne
comprend les mcanismes qui dtruisent les nmatodes que de quelques plantes; le soufre semble jouer un rle important dans les
matires actives lorigine de cette rsistance chez les plantes dorigine agricole. De mme, certaines plantes indignes produisent
des composs alllopathiques qui attaquent les nmatodes. La gestion de la population de nmatodes dans les sols arables par des
techniques de lutte intgre nen est qu ses dbuts, si bien quon doit entreprendre des recherches pour quantifier les effets des
plantes rsistantes et des amendements azots. Un programme de lutte intgre pourrait inclure la culture despces rsistantes,
lusage des fertilisants appropris et la promotion dantagonistes bactriens. Il se pourrait quon doive recourir diverses
mthodes de calcul pour analyser et expliquer les mcanismes de lutte multifactoriels contre les nmatodes. Des programmes de
lutte moins toxiques pourraient favoriser la population de nmatodes qui sattaquent aux arthropodes parasites dans le sol. Enfin,
dautres recherches sur les nmatodes du sol pourraient illustrer lutilit de ces derniers en tant quindicateurs de la vitalit de
lcosystme agricole et de la pollution de lenvironnement.
Mots cls: Lutte biologique, biodiversit, rpartition des nmatodes, gestion des nmatodes, cologie du sol
parasites of whales to microscopic species that invade various plant organs. Whatever the preferred environment, all
nematodes are aquatic in the sense that they exist in water or
moisture films, and must have such surroundings to avoid
desiccation and to breathe, as their oxygen is obtained by
diffusion through micropores in the body cuticle. While esti289
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will be highly improbable in an era when economics determines what research will be attempted and deliverables
must be specified in advance of actual study. However, the
mission should be attempted; as Niles and Freckman (1998)
state Understanding the scales of biodiversity and their
contributions to the structure and function of agroecosystems is basic to understanding the ecology of crop production and pest management.
Biodiversity and Biology
Among the plant-pathogenic nematode species known to
exist in Canada, sufficient variability exists in such fundamentals as the plant organs parasitized, the nature of pathogenesis and the ecology when outside the host, to indicate
that numerous niches are occupied by these nematodes. A
substantial group of species do not enter plant parts at all but
feed in the rhizosphere on root hairs, surface cortical cells,
or by extending feeding organs into meristematic tissue of the
root cap (Criconemoides, Helicotylenchus, Paratylenchus,
Trichodorus, Tylenchorhynchus, Xiphinema). Of those
nematodes that actually enter plant parts, the roots, stems,
bulbs, corms, rhizomes, leaves, and seed ovaries of host
plants may be colonized by species of Aphelenchoides,
Ditylenchus, Globodera, Heterodera, Meloidogyne,
Pratylenchus. Species that invade seed ovaries (Anguina,
Ditylenchus) can subsequently endure extended periods of
adverse climatic conditions in a cryptobiotic dormant state
(Van Gundy 1965). Biological mechanisms promoting the
survival of adverse climatic conditions are equally effective,
when required, in all geographical areas of the distribution
range of a species. Within the soil habitat, mechanisms for
survival of adverse conditions can include the following:
avoidance of freezing by internal storage of body fat as
triglycerides with depressed freezing points, and moderate
desiccation, which will increase the concentration of internal salts and depress freezing points (Sayre 1964); rapid
movement through the soil profile to regions of more conducive soil temperature by Pratylenchus penetrans and
Trichodorus pachydermis (Rossner 1970); mild desiccation
to achieve a state of anhydrobiosis in dry conditions
(Simons 1973; Townshend 1984); modified body structures
that permit the retention of internal moisture in droughts;
and protection from damage in the egg stage by encasing the
eggs in various climate-resistant capsules (Wallace 1968).
Some species are known to have alternate pathways of terminal oxidation that permit temporary survival in anaerobic
conditions, as in flooded soil, or allow them to enter a quiescent state (Norton 1978). Of the soil habitat studies just
mentioned, Sayres (1964) research at the Harrow Research
Station stands out as a uniquely Canadian contribution,
although not the only example of our productivity. At one
time or another, Canadian nematologists have worked and
published on all of the genera and topics just listed.
Another Canadian body of research, on nematode pathogenesis, stimulated interest in the soil activities of
cyanogenic glycosides, such as amygdalin from Prunus spp.
(Mountain and Patrick 1959; Traquair 1984), as nematode
suppressors. Whether these compounds are stress metabolites (= phytoallexins) or simply toxins released as a result
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and Marks (1974) tested the use of transformations for normalizing count data and also investigated the intensity of
sampling of field populations of nematodes. While determining that a log (x + c) transformation was an acceptable
normalizing transformation, these authors also found that in
practical sampling, a set of five samples, each consisting of
40 soil cores, was required to estimate the population of
lesion nematodes in a 0.01-ha plot, with a precision level
such that 95% of the estimates of nematode density were
within 20% of the true mean for the plot. The sampling to
achieve this level of precision would require 7 h per 0.01-ha
plot; hence, our earlier comment about the realism of sampling at finer scales. Proctor and Marks (1974) acknowledged that The distribution of nematode counts is likely to
change not only with sampling method and type of nematode but with plot size, soil type, and types of crop.
Given the concern of Proctor and Marks (1974) and others for normalizing their data, it is interesting that almost
no one has apparently challenged whether the usual statistical assumptions regarding biological distribution, e.g., normality of distributions and randomness, are actually valid in
the real world. However, Norton (1978, p.13) suggested
that nematodes are seldom, if ever, uniformly distributed,
and indicated that the most common pattern of spatial distribution is the cluster. Regarding Sneath and Sokals
(1973) observation that a distribution may be random on one
scale and clustered on another, Norton (1978) commented
something more than root distribution can govern nematode occurrence. More recently, Sohlenius (1993) has also
reported stochastic or chaotic development of forest humus
nematode populations, and Wallace and Hawkins (1994)
have suggested geostatistics (regionalized variable theory)
as a means to study nematode populations. It may be that
these authors are directing nematology toward the concept
that a different set of mathematical assumptions is needed
for dealing with soil organisms, as were Morse et al. (1985).
These reports on clustered or chaotic patterns of spatial and
temporal distribution are reminiscent of the fractal geometry
developed by Mandelbrot (1983). We suggest that fractal
geometry be investigated as a tool to describe nematode spatial and temporal dynamics.
Collections of Nematodes in Canada
The most concerted effort in nematode taxonomy and systematics, and consequently the most extensive collection of
preserved nematode genera and species in Canada, was
made in what was known as the Biosystematics Research
Institute of Agriculture Canada on the Central Experimental
Farm in Ottawa (Ebsary 1991). This collection, when last
catalogued, amounted to ca. 15 000 microscope slidemounts, supported by a computerized database record in
dBase. The slides included both plant-parasitic and nonpathogenic species, a number of which were type specimens
of species first described in this country. The plant-parasitic
specimen collection was representative of the horticultural
areas of the country, but somewhat less so for the field cropping regions, e.g., the Prairies. As well, the collection comprised a substantial number of specimens of free-living
nematodes including hyper-parasitic species of the
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in rhizospheres as being suppressive to nematodes in a variety of ways, frequently by interference with reproduction or
development. Could the results of El-Zawahry et al. (1998)
on P. penetrans development also be related to such bacterial activity?
An entirely new frontier for nematode control has been
developing rapidly in the past decade, with the accelerating
growth of techniques in genetic engineering and molecularassisted plant breeding (Vrain 1999). Incorporating new
toxins into plants, specifically targeting specified nematodes; enhancing hypersensitive plant reactions to nematode
attack; and altering plants to reduce the ability of the nematodes to elicit a feeding cell response are only some of the
potent new approaches. It may be possible to engineer plant
proteins that reduce the reproductive capability of the invading nematode, or to alter the plants to produce anti-feedants.
Transgenic exchanges of various resistance genes between
plant species have already been accomplished. As Vrain
(1998) has noted, plant-parasitic nematodes have not
evolved field resistance against cholinesterase inhibitors in
40 yr, so that genetically engineered control systems may
prove to be fairly durable.
A mirror-view of biocontrol suggests the promising
concept of entomopathogenic nematodes as biocontrols for
a variety of insect pests, a concept actively pursued in the
past five decades by such Canadian nematologists as J. R.
Finney, R. Gordon, W. R. Nickle, J. M. Webster and H. E.
Welch (Nickle and Welch 1984). In their review, Nickle and
Welch (1984) concluded ... the potential for use of entomophilic nematodes as self-perpetuating biological control
agents lies in areas where chemical pesticides are too expensive, not practical, or most noxious to humans and the environment. These situations, such as near water, stream and
ponds... in soil situations like concentrated irrigated or river
bottoms where agricultural production occurs, are also fortunately ideal habitats for high nematode parasitism of
insects. Lately the genera Steinernema and Heterorhabditis
have been under scrutiny as potential narrowly targeted
bioagents against such diverse insects as weevil juveniles,
root-feeding scarab beetle juveniles (white grubs), fungus
gnats, corn earworms, oriental fruit-moth caterpillars and
other Lepidopterans, flea beetles, termites and more
(Gaugler and Kaya 1990). Since this aspect of biocontrol
has developed as a benign alternative to the hard chemical
pesticides, a thriving industry is emerging around these genera and their relatives, with unexpected results. The efficacy
of these nematodes has been shown to result from bacterial
symbionts (Xenorhabdus sp.), which inhabit the intestinal
tracks of the nematodes; toxins from the symbionts are
assumed to cause the death of the targeted insect (Nealson
et al. 1990). Research into the biology of the bacterial symbionts has revealed strains that may produce anti-cancer
agents (Li et al. 1997) and a patented new genus
(Photorhabdus) which is luminescent (Nealson et al. 1990;
Strauss 1998). However, like all other nematodes, the entomopathogenic species require moisture to avoid desiccation,
which is a limitation on the circumstances in which they can
be used as bioagents. Unlike a conventional chemical pesticide, an entomopathogenic nematode species for biocontrol
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must be applied by the user with due regard both for the
probability of drying-out and for the brief time which the
nematode may have to contact and enter the target insect.
Unfortunately, although the existence of entomopathogenic
nematodes has been recognized for many years (Steiner
1929), and attempts have been made to exploit their activity
against insect pests (Jaques 1967; Nickle and Welch 1984),
the technology of using these species as biocontrols is still
very much in a developmental stage (Blair et al. 1999).
Nematodes and Environmental Contamination
Because nematodes are globally distributed, occupy almost
all conceivable habitats, and exhibit a broad range of trophic levels, inevitably they are exposed to most environmental conditions, including most toxic materials from natural
and human sources. This situation was recognized by
Samoiloff (1987), whose research has developed a practical
use of nematodes as ecotoxicological indicators, particularly of air quality. Samoiloff established four classes of toxic
effects of contaminants: Immediate risk to survival; irreversible damage to some physiological process; reversible
damage to a physiological process; and long-term, low-frequency risk to individuals (i.e., teratogenesis, carcinogenesis, mutagenesis). Principally using the free-living soil
nematode Panagrellus redivivus, he has been able to characterize the reaction of the nematode to 25 known toxic
chemicals including solvents, pesticides, metal oxides, and
the naturally occurring fungal toxin Aflatoxin B. While his
review of the topic of nematodes as indicators includes a
few examples of soil-borne species being studied (Bissessar
1982; Leetham et al. 1982), a much greater body of work
exists with marine nematodes as the focus. However, given
that most nematodes are known to have chemoreceptor
organs and a substantial group of soil-inhabiting nematodes, as well as plant-parasitic and animal-parasitic
species, have been shown to have various sugars involved
in the function of these organs (Jansson 1987), it seems that
further progress in using a broader range of soil-inhabiting
species as toxicant detectors should be possible. Indirectly,
Dusenbery (1987) speculated along the same line of
thought, although his mention of various salts and carbon
dioxide as chemo-stimulators of nematodes was more in
consideration of the potential for blocking the process of
pathogenesis by disruption of host-finding, or of mating
disruption. More recently, Barker and Koenning (1998)
cited several examples of advances in detection, by various
nematode trophic types, of soil toxicants such as copper,
cadmium, chromium, arsenic, and pentachlorophenol;
undoubtedly other toxicants will be determined as being
amenable to detection by nematodes. We also should probably consider whether selected nematode trophic types
might be suitable indicators of required minor nutrient levels, such as sulfur.
SUMMARY
Over the half-century of Canadian nematology, soil-inhabiting plant-parasitic nematodes have tended to be the focus for
nematologists. This is understandable, since much of the
research was conducted in government laboratories for the
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