Agriculture, Ecosystems and Environment, 24 (1988) 169-182 169

Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands

Interactions b e t w e e n N e m a t o d e s and V e s i c u l a r -
Arbuscular Mycorrhizae

R.E. INGHAM
Department o/Botany and Plant Pathology, Oregon State University, Corvallis, OR (U.S.A.)

ABSTRACT

Ingham, R.E., 1988. Interactions between nematodes and vesicular-arbuscular mycorrhizae. Agric.
Ecosystems Environ., 24: 169-182.

Nematodes and vesicular-arbuscular mycorrhizal (VAM) fungi often occur in the rhizosphere
and roots of plants and therefore frequently encounter each other. Mycorrhizal fungi benefit the
plant by increasing the absorption of nutrients and water and by protecting the root from soil-
borne diseases. Nematodes can interfere with any of these functions. Vesicular-arbuscular fungi
do not colonize regions infected by endoparasitic nematodes, and nematodes rarely infect regions
colonized by VA fungi. Nematode-mycorrhizal interactions appear to be very specific and highly
dependent on the particular association of plant cultivar, fungal and nematode species, the order
of colonization by the symbionts and the soil nutrient level. Plant-parasitic nematodes generally
reduce the amount of benefit gained by the association with the fungus. However, VA mycorrhizae
usually more than compensate for the amount of nematode damage sustained by non-mycorrhizal
plants, since their function is generally not affected except in close proximity to the nematode
feeding site. Mycorrhizal fungi and endoparasitic nematodes are often mutually inhibitory, each
reducing the population of the other. In other cases, the stimulation of root growth by the fungus
provides greater habitat and nematode populations increase. Some studies have also observed
increased spore production and higher percent root colonization by the fungus when nematodes
were present. Fungal-feeding nematodes may feed on the fungal symbiont to such an extent that
in vitro cultures may be killed and in vivo infections significantly reduced. In some studies, plants
were severely disadvantaged by this grazing pressure on the fungus, while in others plant growth
was not affected. Under heavy grazing pressure by fungal-feeding nematodes, sufficient hyphae
may be destroyed to limit phosphorus uptake to a level inadequate for nodulation in legumes.

INTRODUCTION

N e m a t o d e s a n d v e s i c u l a r - a r b u s c u l a r m y c o r r h i z a e ( V A M ) o f t e n o c c u r to-
g e t h e r in t h e r h i z o s p h e r e a n d r o o t s of p l a n t s a n d t h e r e f o r e f r e q u e n t l y e n c o u n -
ter each other. T h i s is especially t r u e for V A M a n d e n d o p a r a s i t i c n e m a t o d e s ,
since b o t h g r o u p s o f o r g a n i s m s also colonize t h e s a m e area of root tissue. Sea-
sonal d y n a m i c s of n e m a t o d e s a n d m y c o r r h i z a e are similar a n d significant po-

016%8809/88/$03.50 © 1988 Elsevier Science Publishers B.V.

170

sitive correlations have been observed between the increase in numbers of spores
and nematodes through the growing season (Rich and Schenck, 1981 ). Since
mycorrhizae and nematodes are active during the same periods, they overlap
temporally as well as spatially, increasing the probability of biological inter-
actions between these organisms.
Early evidence of possible interactions between VAM and nematodes was
obtained from surveys in which spores and mycelia of VAM were found to be
more abundant in fields free of cyst (Heterodera spp.) or root-knot (Meloido-
gyne spp.) nematodes than in fields where these nematodes were present
(Schenck and Kinlock, 1974). In addition, several studies noted increased
numbers of spores, arbuscules or vesicles when densities of certain root-para-
sitic nematodes were reduced by nematicide treatments (Bird et al., 1974; Rich
and Bird, 1974; Germani et al., 1980; Rich and Schenck, 1981 ). This response
was greater in treatment of nematode-susceptible cultivars than for resistant
cultivars (Schenck and Kinlock, 1974). Bird et al. (1974) suggested that my-
corrhizal potential could be limited in soils chronically infected with plant-
parasitic nematodes, and Rich and Bird (1974) noted that the damage caused
by nematodes may be magnified through their detrimental effects on the as-
sociated plant symbionts.
The results from these studies on field soils prompted several controlled
greenhouse studies to define more clearly the interactions between plant-par-
asitic nematodes and endomycorrhizae.

EFFECTS OF ENDOPARASITICNEMATODESON VA MYCORRHIZAE

The effects of root-parasitic nematodes on spore production by VAM have

been highly variable. Fox and Spasoff (1972) found that Heterodera solana-
cearum Miller & Gray reduced spore production of Endogone gigantea (Nicol.
& Gerd.) by 68% on one tobacco cultivar and by 35% on another. O'Bannon
and Nemec (1979) observed a significant reduction in sporulation of Glomus
etunicatus Becker & Gerd. on rough lemon infected by Radopholus similis
(Cobb) Thorne, and attributed the decrease to reduced mycelial growth in
nematode-infected plants. Spore production of Glomus fasciculatum (Thax-
ter) Gerd. & Trappe was also reduced significantly by Meloidogyne arenaria
(Neal) Chitw., but the amount of reduction was independent of nematode den-
sity (Atilano et al., 1981 ). In contrast, Schenck et al. (1975) observed a trend
for increasing inoculum density of M. incognita (Kofoid & White) Chitw. to
decrease spore production by three species of Endogone on two nematode-sus-
ceptible cultivars of soybean. Yet, in a resistant cultivar, spore density was
increased by the nematode in 4 of 6 treatments, although these differences were
not significant. Suresh and Bagyaraj (1984) also found large but non-signifi-
cant increases in G. fasiculatum spore production on tomatoes infected with
M. incognita. Roncadori and Hussey (1977) observed that M. incognita signif-
icantly increased azygospore production by Gigaspora margarita Becker & Hall
at low fertility on a susceptible cultivar of cotton, and at high fertility on a
 171

resistant cultivar. They suggested that the nematode induced-physiological

conditions that favored sporulation. In similar experiments, Pratylenchus
brachyurus (Godfrey) Filip & Schuur-Stekh. did not affect sporulation (Hus-
sey and Roncadori, 1978) nor did Tylenchulus semipenetrans Cobb {O'Bannon
et al., 1979). Similarly, no effect on spore production by M. incognita was ob-
served for Glomus macrocarpus Tul. & Tul. on a susceptible cultivar of soybean
(Kellam and Schenck, 1980), or for G. margarita or G. etunicatus on peach
(Strobel et al., 1982 ). Spore production by G. fasciculatum was not affected by
M. hapla Chitw. on onion (MacGuidwin et al., 1985) or by Pratylenchus pe-
netrans (Cobb) on navy bean (Elliott et al., 1984). DeSouza (1979) observed
that the effect of M. exigua Chitw. on sporulation of G. margarita was depen-
dent on the coffee cultivar and nutrient level. The lowest spore production was
in a jointly inoculated susceptible cultivar at a low level of phosphorus (P)
while the greatest number of spores were produced in nematode-infected plants
of a resistant cultivar grown in a high level of P. The reason for the inconsistent
results between these studies may be the inherently large variation in spore
count data, such that few significant differences can be noted between treat-
ments. While differences as low as 14% have been shown to be significant
(Atilano et al., 1981), other studies could not demonstrate significance in
changes of 150% (Schenck et al., 1975).
Other parameters of mycorrhizal formation that may be affected by nema-
todes include percentage infection and development of extra-matrical mycelia,
arbuscules and vesicles. DeSouza (1979) found that percentage infection of G.
margarita was 25% greater in resistant cultivars of coffee infected with M.
exigua, but infection was reduced by nematodes in susceptible cultivars. The
percentage infection of tomato by G. [asciculatum was also increased by M.
incognita and M. javanica (Trenb.) Chitw. but only that for M. incognita was
significant. Scutellonema cavenessi Sher significantly decreased infection of G.
mosseae (Nicol. & Gerd. ) Gerd. & Trappe in soybeans by 32% (Germani et al.,
1981 ), and P. penetrans reduced colonization of G. fasciculatum on navy bean
(Elliot et al., 1984). Sikora and Sitaramaiah (1980) reported that the per-
centage infection of G. mosseae on cotton was slightly decreased by Rotylen-
chulus reniformis (Linford & Oliveira). In most studies however, the presence
of nematodes did not significantly alter the percentage infection by VAM (Kel-
lam and Schenck, 1980; Cason et al., 1983; Saleh and Sikora, 1984) or has not
been reported.
The effects of root endoparasitic nematodes on VAM formation often de-
pends on which organism infects the root first. Percentage infection of tomato
by G. [asciculatum was reduced when M. incognita was inoculated 7 days before,
or at the same time as the fungus, but not when inoculated 7 days after the
fungus (Suresh and Bagyaraj, 1984). Pre-inoculation with VAM 4 weeks be-
fore addition of nematodes is often necessary for extensive colonization and
establishment by the fungus (Sitaramaiah and Sikora, 1984). O'Bannon and
Nemec (1979) found that disruption of cortical tissue by Radopholus similis
left little space for colonization by the fungal symbiont and that mycelial growth
172

and vesicle formation were reduced. Similarly, Tylenchulus semipenetrans pre-

vented the formation of vesicles by G. mosseae in nematode-infected feeder
roots of rough lemon, although arbuscules formed normally. New roots not
inhabited by nematodes were colonized rapidly by the fungus, however, and
produced both arbuscules and vesicles before the nematodes invaded (O'Ban-
non et al., 1979). In root-knot infected soybeans, Kellam and Schenck (1980)
observed that galls developed in mycorrhizal roots. Hyphae were observed in
the galls but arbuscules which were once continuous with fungal structures
above and below the gall were decomposing within the gall. Mycorrhizal struc-
tures contiguous to the galls were atypical and characterized by small round
vesicles and lysing hyphae. Appressorium formation and penetration of galled
tissue by G. macrocarpus was never observed. They suggested that physiologi-
cal changes in the root caused by the nematode created an unfavorable envi-
ronment for the fungus.
Grandison and Cooper (1986) found that intercellular hyphae, vesicles and
arbuscules from a mixture of VAM-infecting alfalfa were not affected by joint
inoculation with M. hapla. However, mycorrhizal structures were not found in
cortical tissue in or near nematode-galled tissues. Similar observations were
made for VAM mixtures infecting clover or tomato (Cooper and Grandison,
1986). Roncadori and Hussey (1977) also observed abundant inter- and intra-
cellular hyphae and arbuscules in root tissue distal to nematode galls but not
in gall tissue. It is difficult to determine, from many studies of co-inhabited
roots, if the nematode or the fungus was the first to infect that section of root.
However, the evidence indicates that nematodes may occasionally infect tis-
sues already colonized by the fungus, but that VAM fungi do not successfully
colonize tissue already inhabited by nematodes.

EFFECTS OF VAM ON ENDOPARASITIC NEMATODES

Responses of nematodes to the presence of VAM have also been varied and
may depend on the specific associations, soil nutrient levels and the timing of
observations. Fungal colonization had no reported effect on population devel-
opment of T. semipenetrans (O'Bannon et al., 1979), R. similis (O'Bannon
and Nemec, 1979), S. cavenessi (Germani et al., 1981), M. incognita (Cason
et al., 1983; Strobel et al., 1982), M. hapla (Grandison and Cooper, 1986) or
P. penetrans (Elliott et al., 1984). In other studies, some of these nematode
species increased in number when VAM were present. Schenck et al. (1975)
found that, in general, production of M. incognita juveniles was significantly
greater in mycorrhizal cotton plants but some cultivar-mycorrhizal combina-
tions had an adverse affect on nematode development. Roncadori and Hussey
(1977) observed that G. margarita significantly increased the number of M.
incognita eggs produced on a susceptible cultivar of cotton. They attributed the
increase to increased root production of mycorrhizal plants since the number
 173

of eggs g- 1 root was not affected significantly. On the other hand, Atilano et
al, (1981) recovered more M. arenaria juveniles from grape plants infected
with G. fasciculatum, even though root systems from VAM and control plants
were similar in size. First generation cyst nematodes (H. glycines Ichinohe)
were significantly fewer on soybeans colonized by an isolate of G. fasciculatum
but other VAM had no effect (Francl and Dropkin, 1985). In contrast, num-
bers of second generation females were significantly greater in all VAM treat-
ments. Grandison and Cooper (1986) also found higher densities of M. hap/a
on mycorrhizal plants of a resistant cultivar of alfalfa. In a split-root experi-
ment, Strobel et al., (1982) reported that both numbers of eggs per plant and
numbers of eggs g- 1 root were increased when G. margarita was on the same
or opposite side of the root system from M. incognita. Grandison and Cooper
(1986) observed that a mixture of VAM increased the total numbers of M.
hapla in a resistant cultivar and in a susceptible cultivar of alfalfa at a high
level of P fertilization. Numbers of nematodes g- 1root were decreased by VAM
in both cultivars however.
In contrast, the majority of interaction studies have observed that VAM
decreased populations of endoparasitic nematodes. Fox and Spasoff (1972)
were among the first to discover that these two organisms may be mutually
inhibitory and observed decreases of 25-35 % in populations of H. solancearum
when co-inoculated on tobacco with E. gigantea. Similarly, Sikora and Schon-
beck (1975) found that significantly fewer (75%) M. incognita and M. hapla
juveniles developed into adults in tobacco, oats and tomatoes pre-inoculated
with G. mosseae. Bagyaraj et al. (1979) and Suresh and Bagyaraj (1984) ob-
served that significantly fewer galls of M. incognita or M. javanica developed
when tomato roots were colonized with G. fasciculatum. Galls that did develop
were smaller in size than in plants without VAM. The number of galls of M.
incognita on soybean was also reduced by G. macrocarpus, even though root
systems of VAM plants were larger (Kellam and Schenck, 1980).
Several aspects of the VAM-nematode interactions have been proposed to
explain the reduction of nematode densities by the presence of the fungus.
Hussey and Roncadori (1978) observed no difference in the total numbers of
P. brachyurus per plant but the density of nematodes g- 1 root was less in cot-
ton colonized by G. margarita. They stated that the phenomenon may simply
be due to a dilution effect from larger root systems of VAM plants. However,
most of the nematodes found were within roots that were not mycorrhizal and
only rarely were nematodes seen in cortical tissue colonized by the fungus.
They suggested that perhaps fungi and nematodes compete for habitable space
within the root. The same conclusion was reached by Sikora (1981) who found
that Globodera rostochiensis Wollenweber was reduced in potatoes colonized
by G. fasciculatum. He added that competition for nutrients may also be a
contributing factor. Similarly, M. incognita galls and the level of G. mosseae
colonization in different areas of a tomato root system were correlated nega-
174

tively (Sikora, 1978). Grandison and Cooper (1986) observed that nematodes
were absent from cortical tissue with more than 10% VAM colonization, but
Saleh and Sikora (1984) found that numbers of M. incognita females were not
reduced until colonization by G. fasciculatum was 80% or greater. Meloidogyne
incognita was not influenced by 20-30% colonization of cotton by G. intrar-
adices Schenck & Smith, but 50% colonization significantly inhibited nema-
tode development (Smith et al., 1986b). The authors suggested that competition
for available photosynthate or production of nematicidal compounds was more
important than competition for space, since nematodes were reduced even when
half of the root system was still uncolonized by the fungus.
Reductions of nematode infection in VAM plants has also been attributed
to complex physiological changes caused by the VAM "condition" (Hussey and
Roncadori, 1978; Sikora, 1981). These physiological changes may be mani-
fested in several aspects of the VAM host-nematode parasite relationship which
make the plant more resistant (i.e. less nematode reproduction) to the nema-
tode (Hussey and Roncadori, 1982 ). The changes in root physiology may alter
the attractiveness of roots to nematodes (Sikora, 1978) or present physical or
chemical barriers to penetration (Kellam and Schenck, 1980 ). Penetration of
tomato by M. incognita was affected adversely by G. mosseae since 64% fewer
juveniles successfully penetrated VAM plants (Sikora, 1978). Similarly, sig-
nificantly fewer juveniles of R. reniformis penetrated tomato roots pre-inocu-
lated with G. fasciculatum, regardless of the number of nematodes inoculated
(Sitaramaiah and Sikora, 1982 ). Sikora and Sitaramaiah (1980) observed that
60% fewer R. reniformis penetrated VAM-colonized cotton in 5 days, and 30,
36 and 41% less penetrated VAM-colonized muskmelon, cucumber and bush-
bean, respectively, after 8 days (Sitaramaiah and Sikora, 1981 ). When M. hap/a
and G. fasciculatum were inoculated on onion simultaneously, first-generation
juveniles penetrated roots before the fungus was established. However, by the
time the second-generation juveniles developed, the fungus was well-estab-
lished and penetration was apparently inhibited (MacGuidwin et al., 1985).
Smith et al. {1986b) also observed that fewer juveniles of M. incognita pene-
trated cotton roots infected with G. intraradices. In contrast, more M. incognita
penetrated VAM-colonized cotton in field microplots, although the numbers
of nematodes after 120 days was not different from control plants (Smith et
al., 1986a). Suresh et al. (1985) found no difference in the number of M. in-
cognita juveniles that actually penetrated tomato roots colonized by G. fasci-
culatum. They suggested that pre-infection factors such as components of root
exudates or availability of infection sites were not altered by the fungus.
Physiological changes induced by VAM may also make the root a poorer food
source for nematodes, by producing conditions that are inadequate for opti-
m u m development and reproduction. This is suggested by studies in which
numbers of nematodes or reproduction by nematodes are less per gram of root
biomass in VAM plants (Hussey and Roncadori, 1978; Saleh and Sikora, 1984).
 175

Development of juveniles can be retarded in mycorrhizal plants as soon as

penetration is completed (Suresh et al., 1985). Sikora (1978) found that ju-
venile M. incognita in VAM tomato plants were 63 and 27% smaller 8 and 16
days, respectively, after inoculation than those in non-mycorrhizal plants. De-
velopment of M. incognita was also altered by G. fasciculatum, in that nema-
todes at 5, 20 and 32 days tended to be smaller than in control plants (Suresh
et al., 1985 ). Penetration by R. reniformis juveniles of tomato roots colonized
by G. [asciculatum averaged 9% smaller than those in control plants (Sitara-
maiah and Sikora, 1982). In addition, the body width of females remained
significantly less in VAM-colonized plants. The rate of development from ju-
venile to egg-laying female m a y also be reduced in VAM plants (Smith et al.,
1986b ). Production of gelatinous matrix and egg-laying by R. reniformis were
delayed in VAM plants (Sitaramaiah and Sikora, 1982). After 14 days, all
penetrating females in control plants had egg sacs with an average of 10 eggs
per sac while only 56% of females in VAM plants contained eggs with an av-
erage of only 7 eggs per sac. However, by 30 days there was no significant
difference in number of egg sacs on root systems of control and VAM plants.
MacGuidwin et al. (1985) found that females of M. hapla took 3 days longer
to mature in onions colonized by G. [asciculatum. After 6 weeks, twice as many
penetrating juveniles had developed into adults in non-VAM plants. Between
6 and 10 weeks, the number of hatching juveniles increased in non-VAM plants
but decreased in VAM plants. Saleh and Sikora (1984) observed that increas-
ing levels of colonization by G. fasciculatum in cotton, reduced M. incognita
reproduction. Numbers of eggs were reduced at 55% or greater colonization.
Sikora and Sitaramaiah (1980) also noted less egg production by R. reniformis
on cotton colonized by G. mosseae. Similarly, Strobel et al. (1982) found that
G. margarita decreased numbers of M. incognita eggs produced g-1 of peach
roots grown at a low fertility level. Glomus intraradices decreased nematode
development and egg production more when inoculated 28 days before nema-
todes than when both organisms were added at the same time. When pre-in-
oculated, VAM reduced total eggs produced and number of eggs g- 1 of root but
numbers of eggs per female were not affected (Smith et al., 1986b). Cooper
and Grandison (1986) also found that the numbers of M. hapla on tomato or
clover was decreased more when VAM fungi were inoculated 4 weeks before
the nematode. Presence of the fungal symbionts substantially reduced or com-
pletely suppressed adult development. Similarly, G. mosseae reduced the num-
ber of adult female R. reniformis by 87 and 63% on two cotton cultivars (Sikora
and Sitaramaiah, 1980). Reduced development in VAM ~lants may result from
decreases in available food for nematode growth anew:.eproduction. Suresh et
al. (1985) found that significantly fewer giant cells developed in each gall of
M. incognita. Average cell size was also less than in non-mycorrhizal roots but
this result was not statistically significant. K~l!~m and Schenck (1980) also
suggested that VAM decreased giant-cell development.
176

Physiological changes resulting from VAM formation may actually cause the
root to become antagonistic to nematodes. Suresh and Bagyaraj {1984) noted
that elevated levels of amino acids and sugars observed in VAM roots are as-
sociated with increased plant resistance, each singly or collectively playing a
role in suppressing nematode development. Suresh et al., (1985) found that
50% of M. incognita juveniles exposed to extracts of mycorrhizal tomato roots
died after 4 days. Only 32% of juveniles exposed to either clean tap water or
extracts of non-mycorrhizal plants died during the same period. Suresh and
Bagyaraj (1984) suggested that the presence of nematicidal substances in VAM
roots may result from improved plant vigor owing to enhanced P uptake or
increased concentrations of phenylalanine and/or serine which are known to
be nematicidal.

EFFECTS OF INTERACTIONS BETWEEN NEMATODES AND VAM ON PLANT

GROWTH

The interaction between endoparasitic nematodes and VAM is usually ex-

pressed in either of two types of responses of plant growth or yield. In the first
type {Type I) of response the nematode reduces the growth stimulation caused
by the mycorrhizal symbiont. Plant growth production in the treatment with
nematodes and mycorrhizae is less than in the VAM treatment but greater
than in the control. The closer that value is to the control the stronger the
effect of the nematode on the benefit of the symbiosis. In the second type of
response {Type II), the VAM compensates for part of the growth reduction
caused by the nematode. Plant yield in the treatment with nematodes and
VAM was greater than in the treatment with nematodes but less than in the
control. The closer that yield approaches the control treatment, the stronger
the effect that the VAM has on the pathogenicity of the nematodes. While all
responses may be considered to exist along a continuum of increased plant
tolerance (littlesuppressionofgrowthoryield) (HusseyandRoncardori, 1982),
categorization of experimental results into these basic types facilitates discus-
sion of complex interactions. In a survey of 47 interaction experiments, 45%
were Type I and 34% were Type II. Occasionally (17%), production was great-
est in the treatment with nematodes and VAM and rarely (4%) addition of
VAM to nematode treatments reduced biomass below that with nematodes
alone. Evaluating the significance of these growth responses is difficult since
several of the studies reviewed did not present statistics, and some others may
not have used enough replicates to account for the variance inherent in these
types of interaction studies.
Part of the difficulty in making generalizations about VAM-nematode in-
teractions is related to the parameters measured. While some studies report
above-ground plant biomass, others report fruit or seed yield but rarely are
both reported. Yields may be more sensitive to the interaction between ne-
matodes and VAM than shoot or root biomass (Roncadori and Hussey, 1977)
 177

but may require a longer experimental period a n d / o r special growth condi-

tions. The type of growth response observed and whether that response is sig-
nificant appears to depend on the timing of inoculation and subsequent
observations. Plant responses may be quite different when VAM and nema-
todes are inoculated simultaneously, as opposed to pre-inoculation with VAM
followed by delayed inoculation of nematodes (Cooper and Grandison, 1986;
Grandison and Cooper, 1986). Most endoparasitic nematodes may invade roots
in a few hours to a few days, while VAM fungi may require 10 days to 2 weeks
for successful colonization (Kellam and Schenck, 1980). When inoculated si-
multaneously, nematodes may have the advantage, but when VAM are pre-
inoculated, nematodes may be disadvantaged.

INTERACTIONS BETWEEN NEMATODES, VAM AND NUTRIENT AVAILABILITY

Few studies have examined the interactions between endoparasitic nema-

todes, VAM and nutrient availability. Roncadori a n d Hussey (1977) grew cot-
ton at low and high fertility levels and observed that VAM always had a much
stronger effect on plant growth than increased fertility. The stimulation by
VAM was less with increased nutrient availability but it was reduced by the
same proportion in treatments with or without nematodes. This trend was
basically the same for susceptible and resistant cultivars and for shoot weight
and yield, with the exception that VAM improved yield much more in the sus-
ceptible cultivar. Nutrient level had no significant effect on numbers of ne-
matodes. Hussey and Roncardoni (1978) conducted a similar experiment and
obtained nearly identical results.
Cooper and Grandison (1986) studied interactions between VAM and ne-
matodes at increasing levels of P. In general, VAM had less of a stimulatory
effect as P levels were increased, but the reduction in VAM benefit with added
P was not as great in treatments with nematodes. In addition, there was no
trend for addition of P alone to reduce the relative growth retardation caused
by the nematodes. These results suggested that VAM compensation for ne-
matode-caused growth reduction was a result of more than just added P nutri-
tion. Gigasporamargarita decreased reproduction ofM. incognita, but increasing
the fertility level negated the beneficial function of the fungus (Strobel et al.,
1982). Additional nutrients alone had no effect on nematode egg production.
As in other studies, addition of fertilizer reduced the relative benefit of the
VAM. However, at high fertility, VAM tended to improve plant growth more
in treatments with nematodes. This is similar to the trend cited above and
suggests that nematodes may reduce plant uptake of P so that the VAM plant
perceives an environment of lower P concentration when nematodes are pres-
ent. At low fertility levels, growth responses to addition of VAM were equiva-
lent to addition of 500/tg g-1 of 10-10-10 NPK, but VAM improved uptake of
Fe, Cu and Zn more than additional fertilizer. Thus, although high levels of P
increased growth in non-mycorrhizal plants, nutrient imbalances developed
178

which were ultimately detrimental to plant vigor. In nematode-infected plants,

inoculation with VAM was equal to doubling the rate of N P K but, in contrast
to other studies, additional P was better than inoculating with VAM.
Root-knot nematodes can reduce the number of feeder roots and disrupt
nutrient absorption. Therefore, infection by VAM may improve uptake in ne-
matode-infected plants by a greater relative amount than in plants without
nematodes. Addition of VAM increased P uptake and concentration of P in
tomato shoots more when M. incognita or M. javanica were present than when
these nematodes were absent (Bagyaraj et al., 1979). In contrast, Germani et
al. (1980) concluded that S. cavenessi interfered with P uptake by mycorrhi-
zae. Smith et al. (1986b) found that co-inoculation of G. intraradices with M.
incognita at planting did not increase shoot growth, whereas growth was in-
creased by added P. However, when VAM were allowed to establish for 4 weeks
before nematodes were added, either VAM or P addition treatments increased
shoot growth. While the number of juveniles that penetrated roots of plants
colonized by G. intraradices was reduced, the number that infected roots in soil
with additional P was increased. In addition, while the rate of nematode de-
velopment was decreased by both VAM and added P, the effect was greater for
the VAM treatment. This again supports the view that the effect of VAM is
more than increased plant vigor from improved P nutrition.
DeSouza (1979) found that root-knot nematodes may alter some of the nu-
tritional benefits of VAM. While P uptake was only slightly less with nema-
todes, that of Zn, Bo and Cu uptake was significantly reduced. Suresh and
Bagyaraj (1984) also observed reduced uptake of N, P, K, Ca, Zn and Mn in
M. incognita-infected tomato. These deficiencies were alleviated in the pres-
ence of G. fasiculatum but uptake was not always increased to the level found
in nematode-free plants. In microplot studies, Smith et al. (1986a) observed
that adding P increased the severity of nematode damage in non-VAM colo-
nized plants and increased the benefit of the VAM to nematode-infected plants.
Meloidogyne incognita reduced uptake of Zn, while VAM increased amounts of
Zn in the plants. Additional P alone did not increase Zn uptake as much as it
increased shoot growth, and thus magnified the Zn deficiency. As a result, the
increased severity of nematode injury with additional P may have been related
to Zn deficiency, which was exacerbated by nematodes further inhibiting Zn
uptake. This nutrient imbalance was alleviated through increased Zn uptake
by the VAM. Increased fertilization alone, therefore, does not fully mimic the
essential role of VAM in disease interactions with root-knot nematodes.

EFFECTS OF FUNGAL-FEEDING NEMATODES ON ENDOMYCORRHIZAE

Nematodes which feed on fungi are common inhabitants of the rhizosphere

and have been shown to be important consumers of saprophytic fungi. How-
ever, the effects of mycophagous nematodes on endomycorrhizal fungi has been
 179

investigated little. Clark (1964) found that Deleadenus sp. fed on the external
mycelia of mycorrhizae in Rhododendron with such voracity that it destroyed
the mycelium as fast as it developed. The resulting deficiency in mycorrhizae
made it difficult for cuttings of the plants to become established. Similarly,
Shafer et al. ( 1981 ) demonstrated that Aphelenchoides bicaudatus (Imamura)
Schuur.-Stekh would feed on five isolates of ericoid fungi. Grazing of the fun-
gus by the nematode on agar plates caused the mycelium to become dark, mu-
coid and appressed to the agar within a week. After 6 weeks, the nematode had
reduced the fungal cultures by a third as compared with controls. The mycor-
rhizal isolates grazed by this nematode changed from a gray-brown feathery
appearance to wet, darkened mats with all aerial hyphae destroyed. Mycelial
growth of 5 isolates was reduced to 47-70% of ungrazed controls. Reduction of
mycelial area on the agar plates represented an index for loss of volume of the
mycorrhizosphere cylinder in which hyphae extend beyond the nutrient-de-
pletion zones next to the root. The authors suggested that feeding by nema-
todes on fungal cytoplasm caused hyphal walls to collapse, resulting in
fragmentation of hyphae involved in nutrient translocation, thus reducing the
nutrient availability to the plant. They concluded that under the stress of hy-
phal grazing by nematodes, more quickly growing isolates may be more advan-
tageous to the plant than slow-growing fungi.
Hussey and Roncadori (1981) investigated the relationship between the
fungal-feeding nematode Aphelenchus avenae Bastian and G. margarita and G.
etunicatus on cotton. When 75 or 150 A. avenae per 100 cm 3 soil were added at
the same time, or 3 weeks after addition of G. margarita azygospores, there was
no significant effect on the growth response of shoots as compared with the
controls. However, the higher level of nematodes decreased root growth, re-
gardless of inoculation time or presence or absence of the mycorrhizae. Inoc-
ulation of either density of nematodes at 3 weeks, significantly increased the
final density of azygospores in the soil. At the end of the experiment, nematode
numbers had increased slightly or declined. Best nematode growth occurred
when the nematodes were inoculated 3 weeks after the fungus. In a second
experiment, 250 A. avenae per 100 cm 3 soil had no effect on either shoot or root
growth responses to G. margarita. Inoculum levels of 1000 or 2000 nematodes
per 100 cm 3 soil, however, decreased both shoot and root growth, compared
with the VAM treatment without nematodes. No level of A. avenae had any
affect on root growth of cotton inoculated with G. etunicatus. Final nematode
densities in all treatments were substantially less than inoculated levels. Ne-
matodes had no effect on production of zygospores. Similarly, there was no
effect on percent colonization of roots with either fungus, except for a higher
percent colonization in the G. etunicatus treatment with 1000 A. avenae per
100 cm 3 soil. The authors concluded that any antagonistic relationship of A.
avenae in the field would be limited because of the high densities necessary for
deleterious effects.
180

In contrast, Salawu and Estey (1979) found that the presence of A. avenae
completely negated the growth stimulation by Glomus sp. in soybeans. Mycor-
rhizal plants inoculated with nematodes had smaller leaves and an unhealthy
appearance when compared with treatments with the fungus alone. Aphelen-
chus avenae decreased shoot and root weight in mycorrhizal plants by 40 and
36%, respectively. Spore production was reduced from 75 to 17.5 spores per 250
ml soil. In addition, nodulation of mycorrhizal plants was reduced by 88% when
mycophagous nematodes were present. The authors speculated that the ne-
matodes destroyed sufficient mycorrhizal hyphae, that P uptake was reduced
to an inadequate level for successful nodulation. Aphelenchus avenae had no
effect on non-mycorrhizal plants.
Ingham et al. (1986) found that reduction of nematodes in a shortgrass prai-
rie resulted in 6-10-fold increases in active arbuscular colonization and 1.5-
fold increases in total VAM colonization of blue grama roots. A nematicide,
carbofuran, was used to reduce bacterial-feeding, fungal- feeding and root-feed-
ing nematodes. They suggested that under certain conditions nematodes sig-
nificantly impact colonization of plant roots in field situations, but that
mechanisms which influence this interaction are not well understood.

SUMMARY

Endoparasitic nematodes and VAM fungi are common co-inhabitants of the

roots of plants and are mutually inhibitory. Mycorrhizal fungi do not colonize
regions of roots already infected by nematodes, and nematodes only rarely
infect regions previously colonized by VAM. In plants inhabited by both VAM
and endoparasitic nematodes, nematode populations may be increased as a
result of the larger root systems in mycorrhizal plants but generally nematode
penetration and development is inhibited by VAM. Function of VAM, how-
ever, is not usually affected, except in close proximity to areas of nematode
infection. Plant resistance to nematodes may be increased by VAM but occas-
sionally the fungi have no effect. In some associations, nematodes reduce the
amount of growth stimulation by the VAM while in other studies, VAM fungi
reduce the growth reduction owing to nematode parasitism. Addition of extra
fertilizer does not a!ways mimic colonization by VAM. The type of response
observed depends on the plant cultivar, nematode and fungus species, soil nu-
trient status and the'timing of inoculations and harvest. Much more work is
needed on different cultivar-nematode-VAM fungus associations, grown un-
der a range of environmental conditions, before reliable generalizations or pre-
dictions will be possible.

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