Effects of Earthworms on the Dispersal of Steinernema spp.

Journal of Nematology 27(1):21-28. 1995.
© The Society o f Nematologists 1995.

Effects of Earthworms on the Dispersal of
Steinernema spp.1

D. I. SHAPIRO, 2 G. L. TYLKA, 3 E. C. BERRY, 4 AND L. C. LEWIS5

Abstract: Previous studies indicated that dispersal of S. carpocapsae may be enhanced in soil with
earthworms. The objective of this research was to determine and compare the effects of earthworms
on dispersal of other Steinernema spp. Vertical dispersal of Steinernema carpocapsae, S. feltiae, and S.
glaseri was tested in soil columns in the presence and absence of earthworms (Lumbricus terrestris).
Dispersal was evaluated by a bioassay and by direct extraction o f nematodes from soil. Upward
dispersal of S. carpocapsae and S. feltiae increased in the presence of earthworms, whereas upward
dispersal of S. glaseri was not affected by earthworms. No significant differences were detected in
downward dispersal of S. carpocapsae and S. feltiae in soil with earthworms compared to soil without
earthworms. Downward dispersal of S. gla~eri, however, was greater in soil without earthworms
relative to soil with earthworms. In soil void of earthworms, dispersal of S. glaseri was greatest
followed by dispersal of S. carpocapsae. The presence of earthworm burrows in soil did not influence
nematode dispersal. Nematodes were recovered from the surface, interior, and casts of earthworms.
Therefore, nematodes may have a phoretic association with earthworms.

Key words: earthworm, entomophyllic nematode, nematode, nematode dispersal, Steinernema spp.

Entomopathogenic nematodes in the ge- host presence, temperature, soil texture,
nus Steinernema have many attributes as bi- and soil moisture (14).
ological control agents, including wide
host ranges, safety to nontarget organisms, Dispersal characteristics vary among
and vectoring a bacterium, Xenorhabdus Steinernema spp. Steinernema carpocapsae
sp., which rapidly kills insect hosts (15). (Weiser) moves little from the site of appli-
Despite their great potential as biological cation, whereas S. glaseri (Steiner) is a rel-
control agents, results of nematode appli- atively active disperser (18). Steinernema
cations have been inconsistent (11). Biotic carpocapsae applied to the surface of verti-
and abiotic factors that influence the effi- cal soil columns remained within the up-
per 15 cm after 30 days, but S. glaseri was
cacy of nematode applications must be in- recovered 90 cm below the application
vestigated (8). point (18). Because of these differences in
behavior, S. carpocapsae is classified as an
Increased dispersal may increase the ef- ambusher and S. glaseri is classified as a
ficacy of nematodes against insect pests (9). cruise forager (15). The foraging behavior
Adverse environmental conditions can de- of S. feltiae (Filipjev) is considered interme-
diate between S. carpocapsae and S. glaseri
crease nematode mobility, thereby de- (1). Differences in dispersal behavior may
creasing their effectiveness (8). Factors be important in selecting nematode species
that may affect nematode dispersal include for use against pests occupying different
niches in soil habitats (16).
Received for publication 8 August 1994.
IJournal Paper No. 15954 of the Iowa Agricultural and Interactions with soil invertebrates may
Home Economics Experiment Station, Ames; Project No. increase nematode dispersal (14). For ex-
3130. ample, a phoretic relationship was ob-
2 Department of Entomology, Iowa State University, served between nematophagous mites and
Ames, IA 50011. S. carpocapsae (6). Shapiro et al. (19) re-
ported increased dispersal of S. carpocapsae
Department of Plant Pathology, Iowa State University, in the presence of earthworms. Earth-
Ames, IA 50011. worms are not adversely affected by ento-
mopathogenic nematodes (4,17). There-
4 USDA ARS, National Soil Tilth Laboratory, Ames, IA fore, it may be possible to exploit the asso-
50011. ciation between S. carpocapsae and
earthworms in the soil to increase the effi-
USDA ARS, Corn Insects Research Unit, Ames, IA
50011.

We thank M. Abbas, R. D. Gunnarson, D. Soh, and S. Sou-
hrada for assistancein the laboratory and Drs, I. Glazer, E. E.
Lewis, and J. J. Obrycki for reviewing an earlier draft of this
manuscript. We also thank Dr. G. O. Poinar for nematode
identification. This research was supported in part by the
Leopold Center of Sustainable Agriculture, Ames, IA, Grant
No. 92-18.

21

22 Journal of Nematology, Volume 27, No. 1, March 1995

cacy of the nematode as a biological con- earthworms, Lumbricus terrestris (L.), ob-
trol agent. The influence of earthworms tained from the USDA ARS National Soil
on the dispersal of other Steinernema spe- Tilth Laboratory (Ames, IA), were added
cies and the mechanism(s) of how earth- to the selected columns and allowed to
worms affect nematode dispersal have not burrow for 1 week before nematode appli-
been examined. Because of differences in cation. Subsequently, 10,000 infective ju-
dispersal behavior, the effects of earth- veniles of each species were applied in 0.3-
worms on dispersal may vary among 0.4 ml of distilled water to the bottom sur-
nematode species. Shapiro et al. (19) sug- face of the columns (section 6) to test
gested two hypotheses relating to the upward movement, and to the top surface
earthworm-nematode relationship: the o f the columns (section 1) to evaluate
nematodes are dispersed by direct contact downward movement. Soil columns were
with earthworms and (or) nematodes dis- then incubated for 14 days at approxi-
perse at different rates in soil with earth- mately 21 C and 54% relative humidity,
worm burrows than in soil without bur- after which they were dismantled to eval-
rows. The objectives of this research were uate nematode dispersal.
to determine and compare the effects of
earthworms on dispersal of S. carpocapsae, Nematode dispersal was evaluated using
S. glaseri, and S. feltiae and to investigate two methods: a bioassay against G. mel-
the mechanisms involved in how earth- lonella larvae, and direct extraction and
worms influence nematode dispersal. counting of nematodes. Four replicate soil
columns per treatment were used for each
MATERIALS AND METHODS method of evaluation. For the bioassay,
soil from each column section was re-
The effects of earthworms on dispersal moved and placed in plastic petri dishes
of three nematode species were deter- (150 x 25 ram) with 20 last instar G. mel-
mined in vertical soil columns. Steinernema loneUa (19). The petri dishes were incu-
carpocapsae, All strain, S. glaseri, NC strain, bated at approximately 27 C and 80% rel-
and S. feltiae, strain 27, were originally ob- ative humidity for 72 hours, at which time
tained from biosys (Palo Alto, CA) and nematode-induced larval mortality was re-
were reared in last instars of the greater corded. Mortality was considered to be
wax moth, Galleria meUonella (L.). Experi- nematode induced if cadavers exhibited
mental units were polyvinyl chloride flaccidity and coloration characteristic of
(PVC) pipe consisting of six 4-cm-long sec- Steinernema infections. In the second
tions and 5-cm-d pipe joined with duct method, nematodes were extracted from
tape and filled with soil (34% sand, 28% the soil in each column section using su-
silt, and 38% clay, pH 7.0). Soil moisture in crose centrifugation (13), and Steinernema
columns was adjusted to approximately spp. were quantified by observation with
field capacity. The column sections were an inverted compound microscope at a
numbered vertically; the top section was magnification of x 40.
one and the bottom section was six.
Analysis of nematode movement was ac-
The experiments were organized as ran- complished by determining the number of
domized block designs with depth as a nematodes reaching the half of the column
repeated measure. Experiments testing opposite where the nematodes were placed
upward and downward movement of (sections 1-3 for upward movement and
nematodes were run simultaneously. Six 4-6 for downward movement). Bioassay
treatments (three nematode species, with data were analyzed t h r o u g h ANOVA of
and without earthworms) were each ap- mean numbers of dead G. meUonella larvae
plied to eight soil columns for upward obtained from soil in the three sections op-
movement and eight columns for down- posite to where the nematodes were
ward movement (96 columns total). Two placed. Because differences in virulence
against G. melloneUa among the three

Dispersal of Steinernema spp.: Shapiro et al. 23

nematode species were not determined, in- with S. carpocapsae) were dissected and ex-
terspecific comparisons of dispersal could posed to G. mellonella as previously de-
not be made using the bioassay data. For scribed.
the direct extraction method, ANOVAwas
performed on mean proportions of nema- An additional experiment was con-
todes recovered. Proportions were calcu- ducted to determine whether nematode
lated based on the number of nematodes dispersal is greater in soil with earthworm
recovered from the half of the column op- burrows than in soil without burrows. Up-
posite to where the nematodes were placed ward dispersal of S. carpocapsae was deter-
relative to the total number of nematodes mined in vertical soil columns in an exper-
recovered in that column. Using these pro- iment with a design similar to previous ex-
portions, extraction efficiency for each periments. Soil columns and experimental
species was not a factor; hence compari- conditions were as previously described,
sons of dispersal among Steinernema spp. but treatments were columns with earth-
could be made. If significant differences worms and burrows, columns with bur-
were found with the ANOVA,then multiple rows only (earthworms removed), and col-
range tests (LSD) were used to distinguish umns with no earthworms or burrows.
treatment effects. There were five replications per treatment
(15 columns total). Two earthworms (L.
An experiment was conducted to inves- terrestris) were added to ten randomly se-
tigate whether nematodes were moved lected columns and allowed to burrow for
through soil via a direct contact relation- 1 week, after which five columns were dis-
ship with earthworms. Approximately 1.5 mantled. Earthworms were manually re-
z 106 S. carpocapsae were placed in 3 liters moved from the dismantled columns,
of soil with 10 L. terrestris and incubated at which were then reconstructed with the
27 C for 7 days. Subsequently, the earth- earthworm burrows realigned. Realign-
worms were removed and washed vigor- ment of column sections was accomplished
ously using distilled water. The wash from by aligning straight vertical lines, which
each earthworm was poured onto filter pa- were drawn on the columns prior to sepa-
per in 100 x 15 mm petri dishes. The ration of the column sections. Ten thou-
earthworms were rinsed further in run- sand nematodes were then applied in 0.4
ning tap water, placed in separate petri ml distilled water to each column, and col-
dishes with filter paper, and allowed to cast umns were incubated for 2 weeks as de-
for approximately 1 hour. Five earth- scribed herein. Following incubation,
worms were then placed at -10 C for 7 nematode dispersal was estimated and an-
minutes to immobilize them and were sub- alyzed using the bioassay method de-
sequently cut into 1-cm-long sections; scribed herein. This experiment was re-
nematodes were extracted from the dis- peated with no changes in procedure ex-
sected material through a Baermann fun- cept that all columns were dismantled and
nel (2). The extracted nematode suspen- then realigned, and nematode dispersal
sions were poured onto filter paper in five was evaluated using the direct extraction
petri dishes. Three last instar G. meUoneUa method.
were placed in each petri dish (from the
wash, casts, and dissections), and the petri RESULTS
dishes were incubated at 27 C and 80%
relative humidity. If larval mortality oc- The G. melloneUa bioassays indicated in-
curred, the cadavers were placed on White creased upward dispersal of S. carpocapsae
traps (20) to verify nematode infection. To and S. feltiae in columns with earthworms
test whether a natural population of Stein- relative to columns without earthworms
ernema spp. may have been associated with (Table 1). No effects of earthworm pres-
earthworms, five additional L. terrestris ence were detected using the bioassay
(that were not incubated in soil infested method to determine upward dispersal of

24 Journal of Nematology, Volume 27, No. I, March 1995

TABLE 1. N u m b e r o f d e a d Galleria mellonella larvae f r o m soil c o l u m n s t e s t i n g u p w a r d d i s p e r s a l o f t h r e e
Steinernema spp. in t h e p r e s e n c e a n d absence of the e a r t h w o r m , Lumbricus terrestris.

S. carpocapsae S. feltiae S. glaseri

Section depth (cm) L+ ? L- L+ L- L+ L-

1. 0 - 4 13.5 0.8 7.3 2.8 12.5 17.3
2. 4 - 8 13.8 6.3 7.0 1.3 13.3 19.0
3. 8-12 16.0 12.3 9.3 1.0 16.0 18.3
4. 12-16 13.8 14.0 10.8 2.5 19.5 19.8
5. 16-20 15.5 17.0 19.0 14.0 19.5 19.3
6. 20-24 19.4 20.0 19.8 19.3 19.0 20.0
m:~ = 14.6 a 6.4 b 7.8 b 1.7 c 13.9 a 18.2 a

Numbers represent means of four replications. Nematodes were introduced 24 cm below the soil surface. Twenty G.
mellonella larvae were exposed to soil removed from column sections 2 weeks after nematodes were introduced. Galleria
melloneUa mortality indicates relative nematode densities.

q"L+ = presence and L - = absence of the earthworm, L. terrestris.
~:m = average mortality of G. melloneUa larvae in the top three sections (1-3). Means from within-species comparisons
followed by different letters are significantlydifferent at P ~< 0.05.

S. glaseri (Table 1). Results from the direct seri in the absence of earthworms than in
extraction method evaluating upward the presence of earthworms (Table 4). In-
nematode dispersal followed the same terspecific comparisons indicated down-
trends as bioassay data, but differences be- ward dispersal abilities in the absence of
tween earthworm presence and absence earthworms to be greatest in S. glaseri fol-
were not significant (Table 2). Interspe- lowed by S. carpocapsae. In the presence of
cific comparisons made from direct extrac- earthworms, dispersal of S. glaseri and S.
tion data indicated that in the absence of carpocapsae were comparable and were sig-
earthworms, upward dispersal of S. glaseri nificantly different from dispersal of S. fel-
was greater than dispersal of S. carpocapsae tiae (Table 4).
and S. feltiae (Table 2). In the presence of
earthworms, dispersal of S. carpocapsae was Nematodes were isolated from the sur-
not different than that of S. glaseri. face, casts, and interior of earthworms.
Emerged nematodes were observed in 1 of
Bioassay results indicated no significant 10, 6 of 10, and 5 of 5 White traps that
effect of earthworms on downward dis- contained G. meUoneUa exposed to nema-
persal for the three nematode species (Ta- todes from the wash of earthworm sur-
ble 3). Results of direct extraction indi- faces, earthworm casts, and dissected
cated greater downward dispersal of S. gla- earthw6rms, respectively. The emerged

TABLE 2. N u m b e r o f n e m a t o d e s r e c o v e r e d f r o m soil c o l u m n s testing u p w a r d d i s p e r s a l o f t h r e e Stein-
ernema spp. in t h e p r e s e n c e a n d absence o f the e a r t h w o r m , Lumbricus terrestris.

S. carpocapsae S. feltiae S. glaseri

Section depth (cm) L+~ L- L+ L- L+ L-

1. 0 - 4 28.0 0 3.5 0.5 74.0 222.0
2. 4-8 22.8 0.5 6.0 0 213.5 525.0
3. 8-12 27.0 9.0 10.5 5.0 427.5 614.5
4. 12-16 4.5 28.5 26.0 465.0 530.5
5. 16-20 9.0 52.5 123.0 48.0 904.5 550.5
6. 20-24 34.5 77.5 807.5 478.0 304.0 803.0
p~ = 515.0 7.1 b ~ 2.7 b 0.7 b
18.0 ab 29.5 a 37.5 a

Numbers represent raeans of four replications. NematodEs were introduced 24 cm below the soil surface.
t L + = presence and L - = absence of the earthwoi:ha, L. terrestris.
~-p = mean percentage of nematodes recovered from the top three sections (1-3) relative to the total number of nematodes
recovered. Means followed by the same letter are not significantlydifferent at P ~< 0.05.

Dispersal of Steinernema spp.: Shapiro et al. 25

TABLe 3. N u m b e r of dead Galleria mellonella larvae from soil columns testing downward dispersal of three
Steinernema spp. in the presence and absence of the earthworm, Lumbricus terrestris.

S. carpocapsae S. feltiae S. glaseri

Section depth (cm) L+ t L- L+ L- L+ L-

1. 0 - 4 20.0 20.0 20.0 19.8 10.8 16.0
2. 4-8 19.8 19.8 19.8 20.0 20.0 19.8
3. 8-12 19.3 20.0 19.0 18.8 19.8 20.0
4. 12-16 17.8 19.8 12.0 12.8 19.3 19.8
5. 16-20 18.3 19.3 10.8 16.3 19.8
6. 20-24 19.5 16.3 1.5 16.3 19.5
mS = 18.5 a 18.4 a 4.5 0.8 17.3 a 19.7 a
9.1 b 5.0 b

Numbers represent means of four replications. Nematodes were introduced on the soil surface. Twenty G. mellonella larvae
were exposed to soil removed from column sections 2 weeks after nematodes were introduced. Galleria mellonella mortality

indicates relative nematode densities.
t L + = presence and L - = absence of the earthworm, L. terrestris.
~:m = average mortality of G. mellonella larvae in the bottom three sections (4--6). Means from within-species comparisons

followed by different letters are significantlydifferent at P ~< 0.05.

nematodes were identified as Steinernema tris. In previous research, downward dis-
sp. No Steinernema nematodes were recov- persal of S. carpocapsae was increased in the
ered from the five earthworms that were presence of L. terrestris (19). The reasons
not exposed to soil infected with nema- for discrepancy between previous results
todes. and results reported herein are unknown.
Upward dispersal of S. glaseri was not af-
Dispersal of S. carpocapsae was greater in fected by earthworm presence, but down-
columns with earthworms than in columns ward dispersal was increased when earth-
with earthworm burrows (earthworms re- worms were absent. Reasons for different
moved) and columns without earthworms effects of earthworms on upward and
(Table 5). Dispersal of S. carpocapsae was downward dispersal of these nematode
not different in columns with earthworm species are unclear. Perhaps consistent dif-
burrows compared to columns void of ferences would have been found in up-
earthworms (Table 5). ward and downward nematode dispersal
experiments if more replications had been
DISCUSSION used. Indeed, the trends observed in all
experiments were consistent, regardless of
Upward, but not downward, dispersal of statistical significance. Alternatively, if a
S. carpocapsae and S. feltiae was enhanced phoretic relationship exists between the L.
by the presence of the earthworm L. terres-

TABLE 4. N u m b e r o f n e m a t o d e s r e c o v e r e d f r o m soil c o l u m n s t e s t i n g d o w n w a r d d i s p e r s a l o f t h r e e Stein-
ernema spp. in the presence and absence of the earthworm, Lumbricus terrestris.

S. carpocapsae S. feltiae S. glaseri

Section depth (cm) L+t L- L+ L- L+ L-

1. 0 - 4 83.5 249.0 886.5 1,115.0 47.0 207.0
2. 4--8 58.0 75.0 659.5 737.0 1,171.5 416.0
3. 8-12 36.5 46.5 109.5 198.0 1,082.0 970.5
4. 12-16 15.0 49.0 36.5 621.0
5. 16-20 33.0 43.0 76.5 3.0 590.0 325.0
6. 20-24 30.0 10.5 30.5 6.5 170.0 167.5
pS = 31.5 ab 22.0 b 28.5 2.2 c
93.5 42.3 a
7.3 c 26.5 b

Numbers represent means of four replications. Nematodes were introduced to the soil surface.
t L + = presence and L - = absence of the earthworm, L. terrestris.
:~p = mean percentage of nematodes recovered from the bottom three sections (4-6) relative to the total number of
nematodes recovered. Means followed by the same letter are not significantlydifferent at P ~< 0.05.

26 Journal of Nematology, Volume 27, No. 1, March 1995

TABLE 5. GaUeria mellonella larval m o r t a l i t y f r o m bioassays, a n d n u m b e r s o f S. carpocapsae r e c o v e r e d by
direct extraction, from soil with earthworms, earthworm burrows, and no earthworms.

G. mellonella mortality S. carpocapsae recovered

Section depth (cm) Lt LO 0 L LO 0

1. 0 - 4 3.4 0 0 66.8 0.4 0
2. 4-8 5.2 0.2
3. 8-12 6.6 0 0 18.4 2.8 0.8
4. 12--16 4.6 3.4
5. 16--20 9.4 8.6 0 28.8 3.6 0
6. 20-24 11.6 16.6
mS = 5.1a 0.7b 2.2 6.0 3.6 19.2
p§ =
6.2 21.2 48.0 45.5

14.4 952.4 812.4 300.4

0b

15.0 a 3.1 b 0.3 b

Numbers represent means of five replications. Steinernema carpocapsae were introduced 24 cm below the soil surface. For
bioassay, 20 G. meUonellalarvae were exposed to soil removed from column sections 2 weeks after nematodes were introduced.
GaUeria meUonellamoratlity indicates relative nematode densities.

1"L = presence of two L. terrestris, L0 = burrows present with earthworms removed, 0 = no earthworms or burrows.
:~m = average mortality of G. melloneUa larvae in the top three sections (1-3).
§ p = mean percentage of nematodes recovered from the top three sections (1-3) relative to the total number of nematodes

recovered. Means followed by the same letter are not significantlydifferentat P ~< 0.05.

terrestris and S. carpocapsae and S. feltiae, termediate between S. glaseri and S. carpoc-
then perhaps the nematodes tend to asso- apsae. The disparity may be due to differ-
ciate more with earthworms moving up- ences in soil texture or nematode strain.
ward than with earthworms moving down- Nematode dispersal may be affected by
ward. Steinernema carpocapsae has a natural soil texture; for example, S. carpocapsae
tendency to disperse upwards (10,18). In- dispersal increases with increased soil par-
creased upward, but not downward, dis- ticle size (10). The study of Alatorre-Rosas
persal has been reported previously when and Kaya (1) was conducted in sand,
S. carpocapsae was in the presence of Heter- whereas this research was conducted in soil
orhabditis bacteriophora Poinar, a nematode (34% sand, 28% silt, and 38% clay). In both
species with greater dispersal ability than studies, S. carpocapsae, All strain, was used,
S. carpocapsae (1). but the strain of S. feltiae was not given in
the report of Alatorre-Rosas and Kaya (1).
This research found the natural dis-
persal ability o f S. glaseri to be greater than This study has provided evidence that
that of S. carpocapsae and S. feltiae, which is earthworms may serve as phoretic hosts of
consistent with previous studies confirm- Steinernema spp. Nematode dispersal was
ing the dispersal behavior of S. glaseri as a not different in soil with earthworm bur-
cruiser. Because of the high natural dis- rows compared to soil without burrows,
persal ability of S. glaseri, it is not unex- and results indicated that the relationship
pected that earthworms would not en- between nematodes and earthworms is one
hance dispersal of this species. Perhaps the of direct contact. Steinernema carpocapsae
increased downward dispersal of S. glaseri may be dispersed on the surface of earth-
observed in soil without earthworms rela- worms, or may be passed through the
tive to soil with earthworms may have been earthworm digestive system and remain vi-
caused by earthworm burrows or earth- able. Evidence strongly suggests that the
worms obstructing the paths of these nematodes that were recovered from
earthworms and reared in G. mellonella
nematodes. were the S. carpocapsae that were placed in
This study found the dispersal of S. car- the infested soil, because the nematodes
recovered were identified as belonging to
pocapsae to be greater than that of S. feltiae, the genus Steinernema, and because no
which is contrary to the study of Alatorre- Steinernema were found in earthworms that
Rosas and Kaya (1), in which the authors
found dispersal ability of S. feltiae to be in-

Dispersal of Steinernema spp.: Shapiro et al. 27

were not incubated in soil infested with S. nematodes in genera Heterorhabditisand Steinernema
carpocapsae. Because a high n e m a t o d e con- for an insect host in sand. Journal of Invertebrate
centration was used to bait the soil, addi- Pathology 55:179-188.
tional research will be required to deter-
m i n e to what e x t e n t S. carpocapsae is asso- 2. Ayoub, S. M. 1980. Plant nematology: An agri-
ciated with earthworms in soil with lower cultural training manual. Sacramento, CA: Nemaid
nematode densities. Future studies may Publications.
also determine if other entomopathogenic
species are capable of being dispersed by 3. Berry, E. C., and D. L. Karlen. 1993. Compari-
earthworms through direct contact. son of alternative farming systems. II. Earthworm
population density and species diversity. American
Two methods were used to evaluate Journal of Alternative Agriculture 8:21-26.
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lowed interspecific comparisons. Recent
studies have found that LT50 (time re- 5. Edwards, C. A. 1983. Earthworm ecology in cul-
quired to cause 50% host mortality) and tivated soils. Pp. 123-138 inJ. E. Satchell, ed. Earth-
efficiency of invasion (number of nema- worm ecology from Darwin to vermiculture. London:
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very sensitive methods of evaluating nema-
tode activity (7,12). Perhaps more differ- 6. Epsky, N. D., D. E. Walter, and J. L. Capinera.
ences among treatments would have been 1988. Potential role of nematophagous microarthro-
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E n h a n c e d dispersal o f S. carpocapsae a n d 821-825.
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may improve the efficacy of these nema- 7. Epsky, N. D., andJ. L. Capinera. 1993. Quanti-
todes as biological control agents. The dis- fication of invasion of two strains of Stein~rnemacar-
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carpocapsae is c o m p a r a b l e to that o f S. gla- 8. Gaugler, R. 1988. Ecological considerations in
seri in the presence o f earthworms. Be- the biological control of soil-inhabiting insects with
cause host finding is necessary for success- entomopathogenic nematodes. Agriculture, Ecosys-
ful biological control with nematodes and tems and Environment 24:351-360.
increased dispersal will improve host find-
ing abilities (9), it is important to deter- 9. Gaugler, R., T. McGuire, andJ. Campbell. 1989.
mine if increased earthworm population Genetic variability among strains of the ento-
densities will increase the efficacy of bio- mopathogenic nematode Steinernemafeltiae. Journal
logical control of insects with nematodes. of Nematology 21:247-253.
Additionally, earthworms improve soil
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