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Nematode biodiversity in Canadian agricultural soils

J. W. Potter1 and A. W. McKeown2


1Agriculture

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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

Nematode worms are members of a phylum of unsegmented


invertebrates inhabiting almost all possible environments
worldwide (Thorne 1961). The phylum Nematoda includes
numerous marine species, animal parasites, plant parasites
and saprophagous soil-inhabiting species. Among these
assorted categories, sizes range from macroscopic intestinal

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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mates of the total number of nematode species vary, they are


considered to be second only to the Insecta; consequently the
Phylum can be viewed as ubiquitous on the planet.
Soil-inhabiting Nematodes
Soil-inhabiting nematode worms of both plant-parasitic and
saprophagous types are generally small (12 mm or less)
and transparent. Globally, they are common in almost all
soils, with their distribution being determined by temperature, degree of moisture, and soil particle size, along with
the presence of an acceptable food source. Undoubtedly the
greatest diversity in nematode specialization can be found in
the sub-tropics and tropics, where climate is less of a determinant of distribution, and where the range and severity of
parasitism on all living organisms is greater (Luc et al.
1990). Those species that inhabit the temperate zones and
harsher sub-polar regions have evolved survival mechanisms against freezing injury, while others that exist in hot
dry climates are anatomically adapted for moisture retention
and conservation. A few soil-inhabiting nematodes are
hyper-parasites or predators (Seinura, Mononchidae) on
other soil-dwelling species, whereas some species
(Heterorhabditis,
Neoaplectana,
Neosteinernema,
Steinernema) are entomopathogenic, invading the larval
soil-borne stages of various insects. As well, some species
(Ditylenchus myceliophagus, Aphelenchoides spp.) feed on
the hyphae of fungi, and many of the saprophagous species
(principally Rhabditidae) do not feed on decaying plant
material but consume bacteria in the decaying tissue. Given
this range of trophic habits, it follows that the more the variety of edaphic, floristic and faunistic diversity occurring in
micro-habitats in the soil, the greater the diversity in nematode species and trophic types. Conversely, a soil that is limited in its edaphic conditions is usually deficient in
micro-habitats and so will support a much less diverse
nematode fauna.
THE STATE OF OUR KNOWLEDGE
Much of what is known about nematode distribution in
Canadian agricultural soils is really derived from and mainly applicable to highly artificial conditions created by the
cultivation and cropping of those soils, which have altered
the soil ecology from its original condition. Logically, the
best information on the primeval condition of nematode
populations would be obtained from examination of soils
that have suffered the least possible disturbance by humans
(Barker and Koenning 1998). However, no exhaustive
examinations have been performed in untilled regions; perhaps the closest approximation would be in areas where
long-term naturalization is underway using typical native
plant species (McKeown et al. 1994). As a result, most of
our knowledge has been acquired by the intentional concentration of research on attempted simulation of farming conditions in greenhouse ground beds or pots, or by studying
actively farmed soils, few of which are typical or descriptive
of the original primitive soil state. This circumstance is
unfortunate, since the proclivity to create urban development and housing on the best agricultural land increasingly
forces farming onto less desirable and less well-described

soils, with a consequent tendency for unanticipated pest


problems to occur spontaneously.
An example of this spontaneity developed in the early
1970s when French hybrid grapes (Vitis vinifera) susceptible to tomato-ringspot virus (TmRSV) were planted in the
Niagara Peninsula of Ontario on soil that had originally
been marginal land, including fence-rows supporting native
wild grape (Vitis labrusca) and cherry (Prunus spp.). The
dagger nematode Xiphinema rivesi, a vector of the virus,
was present but had not been economically significant
before because V. labrusca was not susceptible to the virus
(Dias 1977; Ebsary et al. 1984). However the virus-susceptible hybrids were quickly infected through the feeding of
the nematodes, an unforeseen occurrence that severely damaged the reputation of the French hybrids until resistant varieties were identified (Allen et al. 1982).
Comparatively recent efforts at soil management by conservation tillage have further altered the soil physically as a
nematode habitat (Boosalis et al. 1981; McKeown et al.
1998; Webster 1987), as well as increasing the host plant
root growth and therefore the available feeding sites for
nematodes. Parmelee and Alston (1986) found that bacterivore nematodes were significantly more abundant under
conventional tillage than under no-tillage crop management through all seasons, but more fungivores were present
following fall plowing. They ascribed this difference as
related to the rate of development of the respective prey bacteria and fungi under the different tillage systems.
Conventional tillage entails a loss of soil organic matter,
some abrasive effects on the soil biota, and exposure of
organisms deep in the soil profile to heating and drying by
the sun and wind. As a result, beneficial microflora and
microfauna are exposed to considerable disruption, as are
the pathogens. It was observed that conservation tillage
reduced the number of cysts and the damage to wheat in
Australia by Heterodera avenae (Roget and Rovira 1987)
and of Heterodera glycines in the USA (Young 1987); these
results are presumed to be related to changes in the activity
of naturally occurring antagonists.
Overall, the biodiversity of soil-inhabiting nematodes in
Canada is poorly known, as is the biology of some genera.
Notwithstanding selective attempts to describe a number of
genera and species (Sanwal 1961; Wu 1965; Anderson and
Potter 1991; Ebsary 1991) and to determine the distribution
of nematode types of particular interest, such as the family
Mononchidae (Mulvey 1961a, b, 1962, 1963a, b), no definitive studies have established the number of soil-inhabiting
nematode species in this country. At present, no agency
exists with the resources, personnel, or the raison dtre to
attempt anything like a thorough systematic study of the
variety of nematode species that are undoubtedly present in
non-agricultural habitats in Canada. Technically, such a
study would be difficult to initiate, as a result of a paucity of
systematists trained in nematode identification and classification. Physically, to mount such a study would require a
major effort simply to amass the collections of specimens
from the variety of habitats where undescribed species probably occur. As with many areas of science, the mission is not
impossible from the viewpoint of a knowledge base, but it

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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

291

of natural degradation of decaying tissue in soil is unclear.


Certainly some nematode-suppressing plants contain such
glycosides naturally, e.g., dhurrin, a cyanogenic glycoside
in sorghum-sudan (Sotomayor-Rios and Torres-Cardona
1984), linamarin from flax (Linum spp.), and asparagusic
acid from Asparagus sp. However, with particular respect to
amygdalin, the root-lesion nematode P. penetrans is a serious pest of only some varieties of Prunus sp. fruit trees
(Mountain and Patrick 1959) and is able to evade the toxic
effect of this glycoside, depending on its concentration in
the root tissues of the trees. Sensitive varieties react with a
hypersensitive response to nematode probing, presumably
because the nematode hydrolyzes the glycoside, releasing
benzaldehyde and hydrogen cyanide. What is still unknown,
but would be interesting to prove, is whether hypersensitive
Prunus spp. react to P. penetrans by production of enzymes
such as phenylalanine ammonia-lyase (PAL) a key enzyme
in phytoallexin synthesis (Lindgren et al. 1992) or peroxidases (Sijmons et al. 1994), or whether nematode-secreted
-glucosidase (Mountain and Patrick 1959; Townshend and
Stobbs 1981; Townshend et al. 1989) or a combination of
plant- and nematode-secreted compounds interact in pathogenesis when nematodes attack such trees.
Reproductive mechanisms and capacities are also fairly
diverse among nematode species in Canada. Generally,
many ectoparasitic species are parthenogenetic, a strategy
with definite advantages when the individual wanders
through the soil, tending to be solitary and rarely contacting
other members of the species. In contrast, sedentary
endoparasites such as the root-knot (Meloidogyne) and cyst
(Globodera, Heterodera) nematodes, amongst which the
females are generally the sedentary sex while the male is
free-moving outside the root, tend toward amphimictic
reproduction of large numbers of eggs, or if parthenogenetic, the sex ratio may shift toward production of more males
under climatic stresses. Among the migratory endoparasites,
exemplified by the root-lesion nematodes, strategies vary
from one species to another. Pratylenchus penetrans is primarily amphimictic, whereas Pratylenchus neglectus is
apparently exclusively parthenogenetic (Loof 1991). Life
cycles of many important species in Canada have been
described as to the average duration of the developmental
stages, morphological appearance of these, and numbers of
eggs produced, but the longevity of individuals is not well
known, nor are the factors that contribute to longevity or
mortality under non-invasive management. However, the
longevity of several species, as known from research elsewhere (Norton 1978), provides an indication of what might
be expected in our climate. There is little doubt that the biodiversity of soil-inhabiting nematodes of the temperate zone
is not as extreme as among species of sub-tropical regions
(Luc et al. 1990) but the adaptations to the more rigorous
temperate zone climate have still allowed utilization of a
variety of habitats and a broad range of host species.
While the biology of some economically important nematodes in the Canadian climate is fairly well known, for others the knowledge is fragmentary or poorly summarized. As
an example, the most common pin nematode, Paratylenchus
projectus, has been studied with respect to its distribution in

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CANADIAN JOURNAL OF SOIL SCIENCE

Ontario and in eastern Canada (Potter and Townshend 1973;


Willis et al. 1976), in Alberta (Hawn 1973; Webster et al.
1972), and in Quebec (Sutherland 1967) where it parasitized
white cedar, spruces and pines. Its host range in North
America is considered to be wide (Society of Nematologists
1984). The life cycle of this species has not been determined
under Canadian field conditions, although in the United
States in a laboratory agar culture on red clover, maturity
was reached in about 30 d (Rhoades and Linford 1961).
Survival and multiplication of the nematode was observed
in bags of soil stored at 5C for 24 wk (Townshend et al.
1973), implying a tolerance for cool climates; it has been
reported elsewhere to be very tolerant of sub-freezing temperatures (Loof 1975), which could be relevant to its distribution in Alberta. Even though Townshend (1972) found in
greenhouse tests that a population of P. projectus increased
by 100 times in 7 mo on timothy grass, no definite economic loss threshold was determined for the species. However,
on rhubarb, some yield losses were determined with populations from 8000 to 23 000 per kg of soil (Townshend et al.
1973), and field population densities as high as 80 000 per
kg of soil have been detected around gladiolus (Potter,
unpublished). Considerable further study of this nematode
in a coherent program would be required to properly evaluate its significance in the Canadian agricultural scene.
Relatedness and distinction of nematode species can be
problematic, particularly with parthenogenetic species, in
that reproductive isolation is difficult to prove; other techniques are required to characterize true species. Significant
advances have been made in this aspect of taxonomy by
Vrain and co-workers (Petersen and Vrain 1996; Robbins et
al. 1996; Petersen et al. 1997; Blok et al. 1998;
Waeyenberge et al. 2000), using molecular taxonomic techniques with a variety of genera including Pratylenchus,
Meloidogyne, Globodera, Xiphinema and others. As the
training of traditional systematists decreases, and international trade in plant materials including food products and
ornamentals continues to expand, the need for accurate and
rapid identification of pest species increasingly acquires
greater importance. The molecular taxonomic work initiated
by Vrain and co-workers is a valuable new field with a significant future in documenting the diversity and abundance
of Canadian nematode species, including plant-parasitic and
other trophic types of soil nematodes, as well as having utility in rapid detection of potentially dangerous imported
species at commercial entry points.
Endemic or Exotic Evolution of Biodiversity
Another consideration in reviewing the effects of human
disturbance of agricultural soils is that, because of intentional importation of foreign or exotic plant species and consequent accidental introduction of foreign nematode
species, it is now difficult to determine which species were
historically endemic and which are genuinely exotic
(Norton 1978). This is important to our view of biodiversity, since it is frequently the case that an introduced exotic
species will expand in numbers and range of distribution to
a greater extent than might have been expected. This usually occurs because the introduced exotic is no longer under

whatever constraints it may have faced in its original area as


a result of limitations brought about by hyper-parasites or
predators. To manage biodiversity in the face of unrestricted expansion by an exotic introduction becomes a more difficult problem.
Several examples of the point just mentioned can be
found in Canadian nematology, e.g., the pinewood nematode (Bursaphelenchus xylophilus) in New Brunswick,
Quebec, Ontario, Manitoba, Saskatchewan and British
Columbia (Agriculture Canada 1988); the oat-cyst nematode (Heterodera avenae) in Ontario (Putnam and Chapman
1935); the soybean-cyst nematode (Heterodera glycines) in
Ontario (Anderson et al. 1988); the potato-cyst or golden
nematode (Globodera rostochiensis) in Newfoundland and
British Columbia (Orchard 1965); and the southern rootknot nematode (Meloidogyne incognita) in Ontario greenhouses (Townshend 1966). All of these species are believed
to have been introduced by one mechanism or another
involving human commerce, and apparently all found conducive sites for establishment and multiplication in circumstances where no natural biological controls were present. In
the cases of the several cyst nematode species, which tend to
have more restricted ranges of hosts, a biologically satisfying solution is readily at hand, i.e., cease growing the host
plant species. Commercially, such a solution is usually unrealistic to growers of the host crops. Thus, it becomes a
research problem to resolve the difficulty in other ways. For
example, regulatory restrictions have successfully isolated
Globodera rostochiensis on Vancouver Island and in
Newfoundland to date, but controlling the spread of most
other introduced Canadian cyst nematode species has
proven impossible without quarantines. Coincidently, some
apparently endemic cyst nematodes that occur in Canada are
relatively benign; such species as the knotweed cyst nematode (Heterodera weissi) are little more than biological
curiosities.
An appreciation of the potential for evolution of phytopathogenic races in nematode species is important to
understanding certain inherent difficulties in manipulating
soil nematode biodiversity. As an example, the soybean cyst
nematode, long known as a pest in Asia (Hori 1915), is a
highly mutable polyploid species with an extensive host
range in the family Leguminosae, although soybean is its
primary host. The mutability of the species is attributed to
the fact that races are quantitative and determined by gene
frequencies, which may shift by selection within a given
population (Triantaphyllou 1975). Since the introduction
and detection of this nematode species in North America in
the mid-20th century (Winstead et al. 1955), an estimated
16+ races of the nematode have been characterized.
Soybean breeders have been continuously active in attempts
to gain ascendancy; Riggs and Niblack (1993) noted that of
10 000 breeding lines tested, 65 have resistance to one or
more races of the nematode. At present the average period
of sustained resistance of a new soybean variety is about 3
yr (Baldwin and Mundo-Ocampo 1991). It is important to
note that mono-cropping of soybean varieties has added to
the genetic pressure that promotes rapid change of nematode
race in response to plant resistance. An added problem for

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POTTER AND MCKEOWN SOIL-NEMATODE BIODIVERSITY

the breeders is that in some cases resistance genes are linked


with undesirable characteristics such as black seed coat
color, and also that soybeans are grown in a wide range of
geographic areas with varying climates. Unfortunately for
the industry, commerce dictates sales of pure single-variety
aggregate seed lots. Using a mix of resistant, tolerant and
susceptible varieties, grown with a different blend each time
the plant is cropped, could reduce the rate of resistance
breaking, albeit at the expense of a portion of each crop.
This principle is well-known and advocated by practitioners
of integrated pest management for insects, and could be
adopted as Integrated Crop Management by the soybean
industry, except for the dictates of the market. Riggs and
Niblack (1993) also suggested that rotation with non-host
crops, reduced tillage and adjustment of planting date
should be a part of such integrated crop management.
Admittedly, not all nematode species present as complex a
genetic problem as does the soybean cyst nematode, but neither can it be assumed for any species that a breeding program will be the quickest, cheapest, or most enduring
solution. In fact, for many phytopathogenic nematodes,
resistance genes have not been found as yet, and Luc et al.
(1990) believe that their discovery will be more difficult
with migratory endo-parasites like Pratylenchus than with
the sedentary cyst and root-knot species.
Knowledge of Distribution
In this section, we will refer to scales of description of biodiversity; this phrase implies the integration of such parameters as the mixture or diversity of species in a subject area
of specified dimensions, the population density of each
nematode species in that area, the spread of each population,
the clustering or lack of random distribution of species in
the area, and the intensity of sampling of the various
species. Most of the information on distribution of soil
nematodes has been obtained from agricultural soils, and
thus the knowledge base was conditioned by two principal
driving factors, namely, the areas where intensive agriculture has been practiced, and the locations where nematologists have been active in research and surveying.
Concerning the first of these factors, the locations of agricultural soils and of agricultural activity have been well documented. In the century just past, these areas underwent
substantial change as urbanization took agricultural soils out
of production (Clayton et al. 1977), in some cases depleting
the best land, e.g., in Ontario, the Kitchener-Waterloo area
of Wellington and Waterloo Counties or the northern sandy
strip of the Niagara Peninsula from Burlington to Niagara
Falls. Scales of description of the biodiversity of nematodes
in such areas vary with and are adjusted for the purpose for
which the collected data are intended. As an example, for
the purposes of agricultural field research to provide
answers to specific pest control situations, nematologists
commonly might describe the biodiversity on a field-byfield basis, i.e., on a scale involving a few hectares of arable
soil of a farm, with intensive sampling. More extensive
evaluations of the biodiversity would be made over larger
scales, e.g., by County, Region or even by Province, in circumstances where distribution must be known for regulato-

293

ry purposes. A loss of precision could be expected at the


larger scales of evaluation; however, an assumption of
greater precision at finer scales may not be realistic either,
as will be seen later.
As to the second factor, nematology has barely made an
inroad into most of the arable area of the Prairie Provinces,
with the exceptions of the Lethbridge/Olds/Tabor area and
the Peace River valley of Alberta (Webster et al. 1972;
Hawn 1973), and surveys in southern Manitoba (Kimpinski
and Welch 1971). Consequently, the prairie cereal- and
oilseed-growing areas are virtually unknown territory from
a nematological viewpoint. So the knowledge of nematode
biodiversity, emphasizing those species that are phytopathogenic, is mainly from the intensively cropped areas of
British Columbia, Ontario, Quebec, Nova Scotia, New
Brunswick and Prince Edward Island (Willis and Thompson
1967; Kimpinski and Thompson 1990). In these areas,
research on species identification, population densities, and
distribution that was done several decades ago could now be
suspect because of advances in nucleic acid identification
methods, which may contradict identifications made with
light microscopy. Recent surveys (Yu 1997; Yu et al. 1997)
and studies using PCR (Yu and Potter 1997) have shown
some species to occur commonly in soils where previous
work implied they should not be numerous.
For many nematode species in the agricultural soils of
Canada, the knowledge base is quite generalized (Mulvey
1960). Distribution of the more prominent species, such as the
root-lesion nematode Pratylenchus penetrans, is known on a
fairly gross scale from sampling surveys and grower contacts;
such surveys have identified the nematode on 5-mile grids
along major highways in Ontario and elsewhere (Potter and
Townshend 1973; Willis et al. 1976). However, to map nematode species distribution, on the same scale as that used when
soil types were mapped, has been impracticable in terms of
the personnel required. In some cases, several species of the
same genus have been identified co-habiting the same field,
but the interrelationships of these species have not been studied. Neither has research addressed intra-specific or intrageneric competitive effects, or inter-generic competition
among most co-existing nematode species.
As with many other disciplines in biology, nematology
constantly is presented with the challenge of enumerating
individuals and charting their spatial distribution. Sampling
and sampling theory, as well as the mathematics of dealing
with populations and deciding when they are at damaging
levels, underlie many studies in nematology. Two requirements that modellers often try to meet are the prediction of
yield losses for making management decisions, and the prediction of population changes over time. Several recent theoretical publications on these topics have demonstrated the
difficulties in arriving at meaningful approximations of the
distribution of nematodes in space and time (Ferris and
Noling 1987; Prot and Ferris 1992; McSorley and Phillips
1993; Schmidt et al. 1993). Most models developed for the
discipline have been critical point or simulation models,
although McSorley and Phillips (1993) mentioned the problem of dealing with variation such as sampling error. In an
earlier study of this problem of sampling error, Proctor

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CANADIAN JOURNAL OF SOIL SCIENCE

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

Mononchidae. The collection is believed to be intact,


although it has not had a nematologist curator for several
years. As the Canadian National Collection, it should be an
accessible resource, not only for other countries but for
Canadian scientists.
Other smaller collections possibly exist in a few
Agriculture and Agri-Food Canada Research Centers and in
university sites, notably McGill University, Simon Fraser
University, and perhaps in Memorial University in
Newfoundland and at the University of Toronto. It is not
known what collections may exist, primarily because
research centers where nematology was practiced or taught
at one time or another may not have retained slide-mount
collections when the resident scientist retired or departed.
Conservation of Nematodes in Canada
The notion that nematodes might require conservation
would be viewed as a foreign concept by most farmers, agriculturists and foresters who have ever engaged in attempts
to prevent plant damage by the phytopathogenic species of
these animals. Possibly the only current ecological studies
of nematodes, having their conservation as a part of the
goal-set, are a few research projects that are investigating
the use of entomopathogenic or entomophilic nematodes for
control of pest insects, particularly the larval stages of phytophagous Lepidoptera and Coleoptera (Blair et al. 1999;
Riga et al. 2001). It is unknown whether beneficial nematodes, including the entomopathogenic species and the soilinhabiting fungivores and bacterivores, are at serious risk as
a result of agricultural or forestry practices as well as various soil-degrading and soil-polluting practices in urban centers in Canada. Accepting the evidence from other countries
that acid rain may alter population densities of beneficial
predatory nematodes in some cases (Dmowska 1993; Ruess
and Funke 1992) and that tillage can affect nematode communities in agroecosystems (Parmelee and Alston 1996;
McKeown et al. 1998), the time seems opportune to begin
evaluating whether nematode conservation is needed in
agricultural or Boreal areas. The multiplicity of trophic levels at which nematodes function, being primary consumers
(phytophagous), secondary consumers (bacteriophagous;
myceliophagous), and tertiary consumers (omnivorous;
predacious) (De Ruiter et al. 1993; Barker and Koenning
1998), and their consequent effects on nutrient cycling and
plant growth (Ingham et al. 1985), certainly argues that their
conservation is at least as important as that of annelid
worms or other soil fauna.
Biodiversity and Agricultural Productivity
Where nematologists have been active, many of the indications of relationship of species of nematodes with agricultural productivity have been derived from observations on
field associations and cause-and-effect responses to control methods such as soil fumigation. For various reasons,
the extent of nematode pathogenesis as a detriment to crop
yield or quality has not been well established except on
comparatively few crops. One working tool which was
developed to characterize probable crop losses is the economic loss threshold (Olthof and Potter 1972; Barker and

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POTTER AND MCKEOWN SOIL-NEMATODE BIODIVERSITY

Olthof 1976), which is loosely defined as the amount of loss


(or percentage loss) of marketable produce, due to nematode
pathogenesis by nematodes at a specified population density, which would be equivalent to the cost of applying control. As an example, if at a density of 1000 nematodes per
kg of soil, the crop loss is 20% representing $400 per ha, and
if the cost of fumigation is $400 per ha, then the economic
loss threshold is 1000 nematodes per kg of soil. At that number or higher, for that crop, control by fumigation is considered to be an economically viable strategy. Below that
number, fumigation is too expensive for the increased productivity that would be gained as a result of its use. A number of research papers were published in which the use of
the economic loss threshold was central to estimates of
probable crop loss (Barker and Olthof 1976). In most cases,
this application of the threshold was based on single-species
cultures, which did not take into account that the threshold
might change with mixtures of species. More recent
research in other centers has employed similar tools, either
variations on the economic loss threshold as decision-making aids in selecting nematode control options (McSorley
and Phillips 1993; McSorley 1998a), or mathematical tools
such as power laws (Taylor 1961) for population estimation. The estimate that nematodes cause yield reductions
averaging 10% of all crops globally (Society of
Nematologists 1971; Sasser and Freckman 1987) is an indication of the extent of nematode predation of food supplies
and the need for decision-making tools, based on probable
crop loss estimates, for specific farm circumstances. No
estimates comparable in scope to those of Koenning et al.
(1999) have been made for Canadian crops, but would provide a valuable tool for decision-makers.
Since the late 1970s or early 1980s, several injectable soil
fumigant products based on halogenated hydrocarbons have
gradually been withdrawn. Ethylene dibromide (EDB),
dibromochloropropane (DBCP), and some formulations of
methyl bromide are no longer available, as well as the
dichloropropene-dichloropropane mixture sold as DD or
Vidden D. A more-or-less global ban on methyl bromide is due to take effect within the next decade because of
its detrimental effect on the planets ozone layer and consequent inclusion in an internationally agreed list of greenhouse gases; numerous organophosphate and carbamate
products are also losing favor. Obviously, in response to
reduced usage of fumigants as a means of nematode control,
the economic loss threshold is due for re-definition
(Duncan and Noling 1998), although the new base for an
action threshold requires definition. Perhaps a biological
standard could be based on the maximum attainable yield
using an immune crop cultivar, or a crop grown in nematode-free but otherwise normal soil. One quickly recognizes
the problem of finding cultivars immune to many nematode
species, to use as biological standards.
Another consideration in relating biodiversity and agricultural productivity is that it is rare to find a single phytopathogenic species as the sole pathogen in a field. For
instance, in an area previously cropped to tobacco but currently being restored as a naturalized sandprairie using
native-plant species, McKeown et al. (1994) found

295

Pratylenchus penetrans as the most prevalent plant-parasitic


nematode, but also reported lower densities of Meloidogyne
hapla, Criconemoides sp., Tylenchorhynchus sp., and
Paratrichodorus sp. More recently, they have found large
numbers of Paratylenchus projectus and low numbers of
Heterodera sp., Hoplolaimus sp., Rotylenchus sp. and
Xiphinema sp. (Potter and McKeown, unpublished). An
unfortunate but perhaps necessary habit in managing crop
damage has been to recommend remedial actions based on
the numbers of the most prevalent or the most severe single
species of nematode pathogen in the worst affected areas of
an affected field, after determining the population densities
of all of the various nematode species present. In circumstances where several pathogens co-habit in a damaged
crop, determining the extent to which each species contributes to the collective damage and, more importantly,
developing a plan for maximizing crop productivity in
future can be a difficult exercise. This problem was already
recognized at the inception of Canadian nematology
(Hastings and Bosher 1938), and demonstrated further by
subsequent distribution studies of multiple nematode infestations (Olthof and Hopper 1973; Olthof et al. 1982).
Particularly with species that parasitize different plant parts,
or species that inhabit different plants in a mixed-plant crop,
assessing damage is more complicated when loss estimates
are non-additive. As Barker and Koenning (1998) suggested
As information is forthcoming on soil biology, combinations of bacterivorous nematodes and growth-promoting
bacterial species could become diagnostic or keystone
species to assess soil quality and health in sustainable nematode and crop management. Further research with multiplespecies complexes is needed to improve on the ability to
evade crop losses resulting from excessively diverse nematode populations in agriculture. Perhaps a different standard,
one based on the benefits of nitrogen-mineralizing (bacterivorous) nematode species (De Ruiter et al. 1993), would
be a preferable marker of soil biodiversity and soil health.
Biodiversity and Soils Management
From recent research on soil amendments and the fate of
introduced organic materials, it is clear that nematode numbers in the soil can be dramatically altered (Lazarovits, personal communication). Following the example of similar
work in other countries (Stirling 1991), the point is wellproven that agricultural inputs of organic matter, in particular nitrogenous material, will affect nematode populations,
whether directly (Rodriguez-Kabana 1986) or as an indirect
effect of alterations to soil microflora and subsequent alterations of soil chemistry (Rodriguez-Kabana et al. 1987).
What is presently not well understood is the type and quantity of inputs that will achieve a predictable result. Kerry
(1987) strongly advised against field use of large quantities
of soil amendments containing microbial biocontrol agents
against plant-parasitic nematodes, on the grounds that costs
of production, storage and application of such materials
makes their application inefficient and ineffective.
Alteration of relative amounts of supplement mineral elements, which either directly affect the nematodes physiology or which affect plants that have suppressive activity to

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CANADIAN JOURNAL OF SOIL SCIENCE

nematodes as a consequence of release or synthesis of stress


metabolites, is an aspect of soil fertility and quality that has
received attention, but is far from being a predictable and
consistent approach to nematode population management.
Nonetheless, there is good reason to relate host-plant tolerance or resistance to nematodes with plant nutrition
(Trudgill 1992). There are also legitimate reasons to place
nematodes at the focus of nutrient recycling systems (De
Ruiter et al. 1993; Barker and Koenning 1998), since they
function at more trophic levels than most other soil fauna.
Since even the addition of specified minerals in known
quantities to a soil is not a process that at present will produce a consistent, predictable result in respect to nematode
population density, it is possibly premature to attempt to
relate pollutants to alteration in nematode biodiversity and
to consequent changes in agricultural productivity.
However, reports that in some cases acid rain may reduce
beneficial predatory nematodes (Dmowska 1993; Ruess and
Funke 1992) but do not affect plant parasites
(Paratylenchus) and fungivores (Aphelenchoides) give
cause for a certain degree of concern, especially in areas
such as southern Ontario with its high intensity of SO2 emissions and acidic deposition (Smith et al. 1998).
The foregoing should not be construed as implying that
there are no indications of where soil mineral addition or
soil amendments would be likely to have effects on biodiversity in an agricultural context. For example a substantial
body of literature indicates that, among plants that exhibit
nematode suppression, the element sulfur is a common constituent of plant-synthesized chemicals that are known to be
either suppressive or to yield suppressive compounds as
degradation products. Prominent among these are the thiophenes (Uhlenbroek and Bijloo 1959) and polyacetylenes,
and the glucosinolates (Choesin and Boerner 1991). The former two chemical groups are believed to be active by releasing free radicals, whereas the latter degrade to
isothiocyanates, which are known to be severe toxicants as
soil fumigants. Field testing by several groups has demonstrated practical control of nematodes using plants (Tagetes
marigolds; Pennisetum millet; Brassica mustards) that
incorporate sulfur into various chemical constituents (Blair
1999; Kimpinski et al. 2000; Reynolds et al. 2000;
McKeown and Potter 2001). While investigating
cyanogenic cover crops for a number of years in potato rotations (McKeown and Potter 2001), we have wondered why
reported cyanogenic plants did not control P. penetrans very
well and suggested that these crops were in fact hosts of P.
penetrans. Given the relationship of sulfur with these plants,
the fact that cabbage responds well in Ontario to sulfur
applications, and that a potential soil sulfur deficit could
exist concurrent with various changes in sulfur use and
release (Kirchmann et al. 1996; McKeown and Bakker
2000), we suggest that there may be a relationship between
sulfur deficiency and poor control of P. penetrans using
cyanogenic plants. Furthermore, since Bacillus subtilis, a
sulfur-metabolizing bacterium, has been linked with control
of P. penetrans (Utkhede et al. 1992), we wonder how the
sulfur nutrition of bacteria affects P. penetrans directly, or
in combination with acid rain potentially reducing parasites

of P. penetrans. We also wonder why substantial numbers


of P. penetrans females and juveniles, but no males, could
be extracted from the roots of certain cultivars of the
marigolds Tagetes erecta and Tagetes patula after 6 wk
exposure of the plants to the nematodes (El-Zawahry et al.
1998), whereas others have found Tagetes spp. to be nematode-suppressing.
Biodiversity and Biocontrol
More than a decade ago, Stirling (1992) stated Despite the
fact that interest in biological control of nematodes is at an
all-time high, biological control appears to be at least 510
yr away from becoming a practical reality. After making
this comment, Stirling suggested that key areas for research
to achieve his practical reality included: Nematode suppressive soils; pathogenic diversity of antagonists; search
for new antagonists and novel mechanisms of action; selection of rhizosphere-competent antagonists; and understanding the nutritional relationships of each antagonist. When
these key areas are viewed as aspects of a research plan, the
central concept of managing suppression and antagonism
becomes evident, and the degree of difficulty in managing
these actions is readily apparent. The first of these research
areas, nematode-suppressive soils, can be approached either
by introducing selected antagonists to the nematodes natural environment, or by manipulating the antagonists that are
already present. Such a study, by either approach, would
require an appreciation of the nutritional needs of the antagonists, and of their pathogenic diversity. The study of pathogenic diversity alone quickly leads into questions such as:
What is the most virulent isolate available of a given antagonist? Why do isolates differ in virulence? What readily
identifiable markers are there which correlate with virulence? What is the best screening test for virulent isolates?
A comparable set of questions could be elaborated for each
of Stirlings proposed key areas. Stirling summarized his
review thus: I believe we have no alternative but to undertake some systematic, long-term, in-depth studies using
well-monitored glasshouse and field experiments. A similar call for in-depth research was made by McSorley
(1998b), who advised that detailed applied studies to obtain
information that is highly specific for a particular combination of pest and crop in a particular region are required.
Interestingly enough, Atkinson (1889) proposed a range of
tactics for managing root-knot nematode that are strikingly
similar to those presently available: Sterilization of the soil
by starvation of the nematodes, including the use of nonhost
plants; the potential of trap crops; compost; nematicides;
and soil amendments such as hardwood ashes and potash.
One wonders if, a century from now, scientists will still be
debating the same topics.
Several conclusions about biocontrol, which were drawn
by Stirling, are paraphrased here. First, instead of attempting to apply biocontrol agents for immediate effect, as
would be done with chemical pesticides, a more reasonable
approach would be developing their use as a long-term strategy that prevents nematode populations from increasing to
damaging levels; a variant on crop rotation, using naturally
immune plants, would achieve this (McKeown and Potter

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POTTER AND MCKEOWN SOIL-NEMATODE BIODIVERSITY

1994). Next, since nematodes are likely to be distributed in


foci related to the root distribution of the previous crop,
antagonists need to be applied in minimal amounts and at
the optimum position to access the target nematode. Seed
application, for example, or root application on transplanted
crops, would be most efficient. Also, rather than concentrating on a single antagonist species, several antagonists acting
in concert should be more effective, and especially if they
attack different stages of the nematodes life cycle, or act
through different mechanisms. In some soils, as with insects,
chemical nematicides might best be used to reduce a high
nematode population, which is subsequently held in check by
using antagonists, crop rotation, or combinations, stimulated
with additions of appropriate organic amendments.
Conceivably, nematode-tolerant hosts should be grown to
allow a low population of nematodes on which antagonists
can generate higher populations of natural enemies.
A substantial Canadian contribution to the knowledge of
antagonists is the self-published book by Barron (1977); this
work should be read by any scientist aspiring to understand
nematode-suppressive soils. However, even Barron
acknowledged: In most areas related to the physiology of
these [nematode-destroying] fungi, we have barely
scratched the surface... .
The potential for biocontrol involving bacteria has been
emphasized since the early studies of the bacterium
Pasteuria penetrans (Sayre and Wergin 1977; Sayre and
Starr 1988), but has yet to be commercialized. New potential is also thought to exist in the use of rhizosphere-inhabiting bacteria, such as Pseudomonas fluorescens
(Oostendorp and Sikora 1989), although Stirling (1992)
considers that these will probably be commercialized in
combination with other antagonists and control practices.
However, as an example of the possible complications of
Stirlings suggestion, Utkhede et al. (1992) found increased
severity of apple replant disease in the Okanagan Valley
using applications of locally-isolated Bacillus subtilis along
with Pratylenchus penetrans nematodes, but improved tree
growth with applications of B. subtilis in combination with
Trichoderma sp. fungus.
In the context of Stirlings (1992) comments about
selection of rhizosphere-competent antagonists; understanding nutritional relationships of each antagonist; and
novel mechanisms of action, the relationship of rhizosphere-inhabiting bacteria and nematodes may still yield new
insights into biodiversity. For example, the discovery that
genetically altered sweet corn varieties with enhanced
sweetness are better hosts of Pratylenchus penetrans nematodes (Yu and Potter 1998) implies that sugar quantity
and/or quality in the rhizosphere may have been altered in
such varieties. In turn, this could affect sugar-metabolizing
bacterial populations in rhizospheres, possibly including
species like Pasteuria penetrans, Bacillus subtilis, and
Pseudomonas fluorescens, conceivably by affecting chemical signaling involving signal-mimic compounds in the soil
(Bauer 2001). From several research groups (Kimmons et
al. 1990; Kokalis-Burelle et al. 1996; Ball et al. 1997;
Burelle et al. 1999; Gwinn et al. 2000; Weston 2001), evidence is rapidly accumulating, indicating bacterial activity

297

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

benefit of farmers. While many instances of pioneering work


could be cited, it is more instructive to consider the topics
that stand out: Surveys; pathogenesis; cold tolerance; virus
vectors; soilborne hyperparasite taxonomy; soil ecology;
loss thresholds; host ranges; control by fumigation; detection of environmental contaminants; molecular taxonomy;
resistance breeding and evaluation; modes of action of
nematicides; biocontrol. As Canadian soil science and related sciences move into a new millennium, it is safe to say
that none of these topics is now conclusively at a point
where no further work remains. It is also safe to predict that
both natural and synthetic resistance against nematodes
will have a prominent place in agriculture (Vrain 1999).
Canadian soil scientists, microbiologists, and plant pathologists built a strong body of knowledge in the middle decades
of the 20th century. All too often, this knowledge is ignored
or lost because it isnt quickly accessible on data bases or
CD-ROMs. It would be foolish to let previous soils and
agronomic knowledge be wasted or left on the bookshelves,
simply because it cant be found stored on a plastic disk.
Furthermore, many of the ecological studies needed to
develop sustainable cropping systems were done prior to the
advent of electronic search engines. Hence, newer
researchers should make the effort to find this valuable
source of information in the paper-copy literature. This
knowledge ought to be integrated with plant physiology,
crop management and sustainable cropping systems to
ensure the food supply in future. The research topics listed
above, along with more emphasis on rhizobacteria, natural
products chemistry, nematode physiology, and above all an
appreciation of the nematode as an aquatic invertebrate animal (not simply a disease incitant!) will be required in the
next century and beyond.
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Pinewood
nematode,
Bursaphelenchus xylophilus (Steiner and Buhrer) Nickle. Pages
3335 in Summary of plant quarantine pest and disease situations
in Canada, 198788. Plant Protection Division, Agriculture
Canada, Ottawa, ON. 68 pp.
Allen, W. R., Dias, H. F. and van Schagen, J. G. 1982.
Susceptibility of grape cultivars and rootstocks to an Ontario isolate of tomato ringspot virus. Can. J. Plant Pathol. 4: 275277.
Anderson, R. V. and Potter, J. W. 1991. Stunt nematodes:
Tylenchorynchus, Merlinius and related genera. Pages 529586 in
W. R. Nickle, ed. Manual of agricultural nematology. Marcel
Dekker Inc, New York, NY.
Anderson, T. R., Welacky, T. W., Olechowski, H. T., Ablett, G.
and Ebsary, B. A. 1988. First report of Heterodera glycines on
soybeans in Ontario, Canada. Plant Dis. 72: 453.
Atkinson, G. F. 1889. A preliminary report upon the life-history
and metamorphoses of a root-gall nematode, Heterodera radicicola (Greef) Muller and the injuries caused by it upon the roots of
various plants. Bull. Alabama Polytech, Institute, NS. No. 9.
Baldwin, J. G. and Mundo-Ocampo, M. 1991. Heteroderinae,
cyst- and non-cyst-forming nematodes. Pages 275362 in W. R.
Nickle, ed. Manual of agricultural nematology. Marcel Dekker Inc,
New York, NY.
Ball, O. J.-P., Bernard, E. C. and Gwinn, K. D. 1997. Effect of
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