Potential for Entomopathogenic Nematodes in Biological Control:
A Meta-Analytical Synthesis and Insights from Trophic Cascade Theory
Robert F. Denno,
1,2
Daniel S. Gruner,
1
Ian Kaplan
3
Abstract: Entomopathogenic nematodes (EPN) are ubiquitous and generalized consumers of insects in soil food webs, occurring
widely in natural and agricultural ecosystems on six continents. Augmentative releases of EPN have been used to enhance biological
control of pests in agroecosystems. Pest managers strive to achieve a trophic cascade whereby natural-enemy effects permeate down
through the food web to suppress host herbivores and increase crop production. Although trophic cascades have been studied in
diverse aboveground arthropod-based systems, they are infrequently investigated in soil systems. Moreover, no overall quantitative
assessment of the effectiveness of EPN in suppressing hosts with cascading benefits to plants has been made. Toward synthesizing
the available but limited information on EPN and their ability to suppress prey and affect plant yield, we surveyed the literature and
performed a meta-analysis of 35 published studies. Our analysis found that effect sizes for arthropod hosts as a result of EPN addition
were consistently negative and indirect effects on plants were consistently positive. Results held across several different host metrics
(abundance, fecundity and survival) and across measures of plant performance (biomass, growth, yield and survival). Moreover, the
relationship between plant and host effect sizes was strikingly and significantly negative. That is, the positive impact on plant
responses generally increased as the negative effect of EPN on hosts intensified, providing strong support for the mechanism of
trophic cascades. We also review the ways in which EPN might interact antagonistically with each other and other predators and
pathogens to adversely affect host suppression and dampen trophic cascades. We conclude that the food web implications of
multiple-enemy interactions involving EPN are little studied, but, as management techniques that promote the long-term persis-
tence of EPN are improved, antagonistic interactions are more likely to arise. We hope that the likely occurrence of antagonistic
interactions in soil food webs should stimulate researchers to conduct field experiments explicitly designed to examine multiple-
enemy interactions involving EPN and their cascading effects to hosts and plants.
Key words: biological control, crop yield, EPN, food-web dynamics, intraguild predation, interspecific competition, meta-analysis,
multiple-enemy interactions, pest suppression, trophic cascade.
The objective of biological control in production ag-
riculture is to maximize the effectiveness of the natural-
enemy complex in suppressing pests and ultimately in
enhancing crop yield (DeBach and Rosen, 1991; Norris
et al., 2003). Thus, pest managers seek a strong trophic
cascade whereby natural-enemy effects permeate down
through the food web to increase crop production (De-
Bach and Rosen, 1991; Rosenheim et al., 1995; Polis et
al., 2000; Snyder et al., 2005). In an ecological context,
?trophic cascades? are predator-prey interactions that
indirectly alter the abundance, biomass or productivity
of a community across more than one trophic link in a
food web (Carpenter and Kitchell, 1993; Pace et al.,
1999; strict definitions are concerned only with biomass
responses, see Polis et al., 2000; Shurin et al., 2002).
Many factors, however, can alter the strength of trophic
cascades and the extent to which natural-enemy effects
on lower trophic levels either attenuate or propagate
(Schmitz et al., 1997, 2000; Halaj and Wise, 2001; Finke
and Denno, 2004; Gruner, 2004; Borer et al., 2005;
Finke and Denno, 2006). These factors include mul-
tiple natural-enemy interactions (e.g., intraguild preda-
tion and predator complementarity), the peculiarities
(i.e., identity) of predators or parasitoids, the spatial
and temporal dynamics of predator-prey and parasite-
host interactions, interspecific competition, the pres-
ence of alternative prey, habitat structure, physical dis-
turbance, and the quantity or quality of abiotic re-
sources (Hochberg, 1996; Chalcraft and Resetarits,
2003; Borer et al., 2005; Finke and Denno, 2005; Wilby
et al., 2005; Casula et al., 2006; Finke and Denno, 2006;
Schmitz, 2007; Otto et al., 2008).
For example, in the arena of biological control, a
longstanding debate considers whether better pest sup-
pression is achieved by releasing or encouraging one vs.
several natural enemies (DeBach and Rosen, 1991;
Rosenheim, 1998; Denoth et al., 2002; Cardinale et al.,
2003; Stiling and Cornelissen, 2005; Snyder et al.,
2006). The issue remains controversial and system-
specific because there is extensive evidence both for
(Heinz and Nelson, 1996; Riechert and Lawrence,
1997; Symondson et al., 2002; Snyder et al., 2006) and
against (Rosenheim et al., 1993, 1995; Snyder and Wise,
1999; Snyder and Ives, 2001; Prasad and Snyder, 2004)
the proposition that multiple enemies are more effec-
tive than single enemy species in reducing pest popu-
lations. The key to understanding when and where a
natural-enemy complex promotes or relaxes prey sup-
pression likely lies in the sign and strength of interac-
tions among the predators themselves. For example,
multiple enemies can interact synergistically to en-
hance prey suppression (Soluk, 1993; Losey and
Denno, 1998) additively (Chang, 1996; Straub and
Snyder, 2006) or antagonistically, whereby they con-
sume each other (intraguild predation) or interfere
with each other?s capture success (Rosenheim et al.,
1995; Finke and Denno, 2003; Prasad and Snyder,
2004). In some cases, however, complex-structured
habitats provide spatial refuges from intraguild preda-
Received for publication September 5, 2008.
1
Department of Entomology, University of Maryland, College Park, MD
20742.
2
Deceased
3
Department of Entomology, Cornell University, Ithaca, NY 14853.
Symposium paper presented at the 46
th
Annual Meeting of the Society of
Nematologists, July 28?August 1, 2007, San Diego, CA.
The authors are grateful to Richard Lewis for technical assistance and Glen
Stevens for organizing the special issue.
Email: dsgruner@umd.edu
This paper was edited by David Bird.
Journal of Nematology 40(2):61?72. 2008.
? The Society of Nematologists 2008.
61
tion and increase the effectiveness of the predator com-
plex (Finke and Denno, 2002; Denno and Finke, 2006;
Finke and Denno, 2006). Such evidence provides en-
couragement to pest managers that the effectiveness of
the natural-enemy complex can be enhanced via habi-
tat manipulations (Landis et al., 2000; Gurr et al.,
2004).
Most studies of multiple-enemy interactions have as-
sessed their consequences for prey density or parasitism
rate but they have not examined how such interactions
propagate to enhance or reduce plant biomass or yield,
a question of paramount importance in agriculture and
biological control. Importantly, there are some studies
showing that the effects of multiple-enemy interactions
cascade down to basal resources with variable conse-
quences for plant biomass and yield. For instance, in-
tense intraguild predation in a system can relax prey
suppression and dampen the potential cascading ef-
fects of enemies on plant biomass (Finke and Denno,
2005). In contrast, if enemies complement one another
and thus act in concert to suppress prey, enemy effects
can cascade to primary producers, resulting in in-
creased yield (Snyder and Wise, 2001; Casula et al.,
2006).
The great majority of terrestrial studies testing evi-
dence for enemy-propagated trophic cascades have fo-
cused on arthropods or vertebrates as predators in
aboveground food webs (Rosenheim et al., 1995;
Schmitz et al., 2000; Halaj and Wise, 2001; Shurin et al.,
2002; Snyder et al., 2005). Soil-dwelling organisms com-
prising belowground food webs have been virtually ig-
nored (but see Mikola and Set?l?, 1998; Wardle et al.,
2005). Nematodes, despite their prevalence in both ag-
ricultural habitats and natural systems (Sohlenius,
1980; Sasser and Freckman, 1987; Stanton, 1988), are
highly under-represented in studies of population and
food-web dynamics and in particular in those investi-
gating trophic cascades (Stuart et al., 2006). A notable
exception involves the entomopathogenic nematode
(EPN) Heterorhabditis marelatus and its ghost moth host
Hepialis californicus that bores in the roots of bush lu-
pine (Lupinus arboreus) in sand-dune habitats of coastal
California (Strong et al., 1996, 1999; Preisser, 2003;
Ram et al., 2008a). In this natural system, soil mois-
ture promotes EPN survival, which inflicts widespread
mortality on root borers that in turn releases bush lu-
pines from herbivory. Under this scenario, bush lupines
thrive, providing a clear example of how EPN can in-
duce a trophic cascade in a natural, belowground food
web.
Entomopathogenic nematodes in the families Stein-
ernematidae and Heterorhabditidae have been used to
suppress populations of pest insects in a variety of
agroecosystems, and in several cases their positive ef-
fects on crop yield have been shown (Lewis et al., 1998;
Mr?c?ek, 2002; Georgis et al., 2006). Thus, there is evi-
dence for strong trophic cascades initiated by EPN in
agroecosystems. Moreover, EPN are known to interact
antagonistically with other competitors, such as ento-
mopathogenic fungi (Barbercheck and Kaya, 1991), as
well as predaceous nematodes, arthropods, parasitoids
and nematophagous fungi (Kaya and Koppenh?fer,
1996; Sher et al., 2000; Mr?c?ek, 2002; Stuart et al.,
2006), and soil factors can influence EPN-host interac-
tions (Portillo-Aguilar et al., 1999; Gruner et al., 2007).
However, the literature on the subject is widely scat-
tered, and we know little about how EPN interact with
other natural enemies in the system and habitat struc-
ture (e.g., soil characteristics) to affect prey suppression
with cascading effects to plants. Based on our knowl-
edge of aboveground arthropod food webs, such infor-
mation is critical for understanding when and under
what conditions EPN might act as effective biological
control agents.
Toward synthesizing the available information on
EPN and their ability to suppress prey and affect plant
damage and yield, we surveyed the literature and per-
formed a meta-analysis of the data. Meta-analysis is a
statistical method that combines results from indepen-
dently conducted experiments (Gurevitch and Hedges,
1999). Meta-analysis allows for the estimation of the
magnitude of effect sizes (e.g., log ratios) across studies
and can be used to determine if the overall effect (EPN
augmentation in this case) is significantly different
from zero. Our study was designed to test the effect of
EPN on lower trophic levels. Specifically, we calculated
effect sizes to quantitatively assess the impacts of EPN
on: (i) herbivore/pest density or mortality, (ii) herbi-
vore damage, or plant growth, biomass, survival or
yield, and (iii) the strength of the correlation of these
two factors. In line with trophic cascade theory, we hy-
pothesized that EPN additions should have net negative
effects on host population parameters and net positive
effects on plants. We also expected these effects to be
negatively correlated, such that stronger host suppres-
sion leads to more positive cascading effects on plants.
We then review the major factors expected to attenuate
or enhance the strength of cascading interactions
based on our limited knowledge of soil ecology and
more extensive ecological experimentation from above-
ground systems. We also consider how the unique life
history traits of EPN (e.g., restricted dispersal ability
and foraging strategies) might influence the spatial
coupling of EPN-host interactions and thus the prob-
ability for trophic cascades. Altogether, our meta-
analytical approach aims to integrate our current un-
derstanding of the important role entomopathogenic
nematodes play as drivers in food-web dynamics and
biological control.
MATERIALS AND METHODS
Criteria for identifying and selecting studies for meta-
analysis: Published studies testing for EPN indirect im-
pacts on plants were compiled using several different
62 Journal of Nematology, Volume 40, No. 2, June 2008
approaches. First, we surveyed the literature from pre-
vious reviews of experimental studies where EPN were
supplemented to a system or not (e.g., Lewis et al.,
1998; Mr?c?ek, 2002). Next, we used the database Web
of Science to identify all studies that cited EPN review
papers. Last, we performed keyword searches on Web
of Science pairing ?[entomog* or entomopath*] and
nematode*? with various combinations of the following
terms: prey suppression, pest density, biological con-
trol, and plant biomass, damage, or crop yield. Searches
revealed numerous experimental studies with quantita-
tive impacts on arthropod hosts and possible indirect
effects on plants. Because meta-analysis requires quan-
titative data on experimental outcomes (minimally,
means; ideally, variances and sample sizes), published
studies with incomplete designs or qualitative response
variables were discarded.
Additionally, we applied the following a priori con-
ditions for the inclusion of studies in our analysis: (i)
EPN manipulated at one or more application levels,
with an appropriate control lacking EPN addition; (ii)
experiments performed in the field or in large meso-
cosms (e.g., glasshouse)?laboratory microcosm ex-
periments were excluded; (iii) EPN applied only to soil
environments (i.e., experimental foliar sprays were ex-
cluded); (iv) some measure of plant above- or below-
ground biomass, production, yield, damage or mortal-
ity reported. These criteria narrowed considerably the
number of studies that could be included in the analy-
ses, and they limit our inference to broad trends. We
also included three studies in which primary producers
were commercial fungi and compared these results
with plants for any strong deviations. Given the above
criteria, our search resulted in a total of 35 studies of
EPN indirect effects on plants or fungi extracted from
22 publications (see Table 1 for a list of all studies used
in our meta-analysis).
We defined a study as a temporally and spatially dis-
tinct experiment with consistent controls. Multiple
studies could be reported from within one publication
if the same experimental treatments were performed in
different years or in multiple, independent locations
with differing physical and/or biological conditions.
When multiple response measures were reported over
time from the same experiment, we used the last tem-
poral sample. Numerous studies used multiple EPN ap-
plication rates and/or crossed these treatments with
additional factors (e.g., fertilization, watering). When
multiple application levels were used for any EPN treat-
ment, we used results from the treatment combinations
with the highest application rates. We assessed addi-
tional treatment combinations case by case. In studies
where treatments were immaterial to our study, we ex-
cluded inappropriate levels (e.g., treatments lacking
hosts). In cases where no a priori decisions could be
made (e.g., application of EPN by drip irrigation vs. soil
drenches), we calculated effect sizes for each and used
the mean value for the study.
We accepted the following treatment response cat-
egories: abundance or fecundity (hosts); biomass, dam-
age, growth or yield (plants); and percent mortality or
survival (both hosts and plants). Log response ratios
could be constructed if variables were measured with
the same units in any treatment comparison. Where
multiple acceptable measures were reported, or re-
ported for different life history stages (larvae and
adults), we included all acceptable measures and cal-
culated mean standardized response ratios for each
study. Data were extracted from tables or digitized fig-
ures using the GrabIt! XP add-in for Microsoft Excel
(Datatrend Software Inc.).
Calculation of effect sizes: The impacts of EPN on host
and plant variables were assessed by calculating an ef-
fect size for each pair-wise treatment (EPN addition
and control). Because it was necessary to compare re-
sponses using different response measurements and
units, we standardized comparisons among experi-
ments using log response ratios (ln[EPN treatment/
control]). The log response ratio (LRR) is one of the
most commonly used effect metrics in ecological meta-
analysis (Hedges et al., 1999; Lajeunesse and Forbes,
2003). Another commonly used metric, Hedge?s d,
requires a measure of sample variability and weights
individual studies by this variance. This require-
ment would disqualify many studies that were otherwise
appropriate but did not report variability (e.g., %
mortality). Log response ratios require only the
means of any measurement for treatment and control
groups. Moreover, distributions of log ratios typically
conform to normality assumptions, making them suit-
able for a wide range of parametric statistical tests
(Hedges et al., 1999).
The control group was designated as the ambient
environment, whereas the treatment group received
supplemental EPN. Thus, we hypothesized that EPN
addition should result in negative effect sizes for arthro-
pod host population abundance, fecundity or survival,
and these negative host impacts should result in posi-
tive indirect effects on plant biomass, growth, yield or
survival. Negative population variables, such as mor-
tality or plant damage, were multiplied by (?1) to be
directly comparable with positive population effect
sizes.
Analyses of effect sizes: The aggregate univariate LRR
for plant and insect host responses were tested against
the null hypothesis that effects did not differ from zero.
We used simple 1-sided, one-sample t-tests, expecting a
priori that host effects would be less than zero and plant
responses would be greater than zero, as expected by
trophic-cascade theory. We restricted these tests to the
aggregate summaries because of sample size limitations
within smaller response categories (e.g., host mortality
n = 1). We also examined the bivariate association be-
Cascading Effects of EPN Additions: Denno et al. 63
tween host and plant LRR, fitting a linear regression to
this relationship. Thus, we assessed if the strength of
the adverse effect of EPN on hosts was associated with
an increasing positive effect on plant survival or yield.
All analyses were run in the R package (R Development
Core Team, 2008).
RESULTS
Our search yielded a total of 35 studies of EPN indi-
rect effects on plants or fungi extracted from 22 publi-
cations. In these studies, a range of EPN species were
added as augmentative treatments in concentrations up
to 500,000 individuals/m
2
. A variety of steinernematid
(S. feltiae, S. carpocapsae, S. riobrave, S. scapterisci) and
heterorhabditid (H. bacteriophora, H. marelatus, H. sp.)
nematodes were added to suppress a diversity of insects
in four orders (Table 1).
As hypothesized from trophic-cascade theory, effect
sizes for arthropod hosts as a result of EPN addition
were consistently negative (overall 1-sided t = 7.18, df =
32, p < 0.0001) and indirect effects on plants were con-
sistently positive (overall 1-sided t = ?5.1593, df = 22,
p < 0.0001). These results held across several different
metrics for hosts (abundance, fecundity, survival and
? [mortality]; Fig. 1A) and across numerous plant pa-
rameters as well (biomass, growth, yield, survival,
? [damage],and? [mortality];Fig.1B).However,sample
sizes for some response categories were too small for
statistical analysis. The two studies that measured yield
of fungi (Grewal and Richardson, 1993; Grewal et al.,
1993) showed similar impacts on hosts but minimal ef-
fects on mushroom yield (average LRR
host
= ?2.39;
LRR
plant
= 0.024) and did not respond as did the bulk of
plant studies. Therefore, these studies were not in-
cluded in analyses of plant responses to EPN additions.
The relationship between plant and host effect size
was strikingly and significantly negative, as expected by
the mechanisms underlying trophic cascades (R
2
=
0.39, df = 18, p = 0.003; Fig. 2). That is, the measured
positive impact on plant responses generally increased
as the negative effect of EPN on hosts strengthened.
DISCUSSION
Evidence for EPN-generated trophic cascades
Results of our meta-analysis of experimental field
studies provide strong evidence that EPN can reduce
populations of their insect hosts by adversely affecting
host fecundity and survival (Fig. 1A). Our analysis also
shows that EPN effects often cascade to benefit basal
resources in both natural and agricultural systems (Fig.
1B). For example, applications of Steinernema feltiae ef-
fectively reduced populations of the cabbage root flies
Delia radicum and D. floralis, which in turn resulted
in a two- to three-fold increase in cauliflower yield
(Schroeder et al., 1996; V?nninen et al., 1999). How-
ever, EPN do not always promote trophic cascades, and
reductions in plant damage do not always translate into
increased crop yield. Applications of Steinernema carpo-
capsae, for instance, can reduce carrot weevil damage by
59% (Belair and Boivin, 1995), but such EPN applica-
tions do not necessarily result in increased carrot sur-
vival or yield (Miklasiewicz et al., 2002). Moreover,
there are cases in which applications of EPN in crop-
ping systems fail to inflict significant host mortality or
enhance yield (Mr?c?ek, 2002; Georgis et al., 2006).
Thus, we can ask what factors influence the probabil-
ity for EPN-induced trophic cascades. The answer likely
lies in unraveling the complex biotic interactions in-
volving EPN that exist in soil-based food webs and in
elucidating how abiotic factors mediate the strength
and spatial extent of these biotic interactions. In above-
ground terrestrial systems, multiple-enemy interactions
(e.g., omnivory and intraguild predation), resource
competition, habitat structure and physical disturbance
are known to alter the impact of arthropod enemies on
herbivores and their indirect effects on plants (Fagan,
1997; Rosenheim, 1998; Chalcraft and Resetarits, 2003;
Finke and Denno, 2005; Casula et al., 2006; Finke and
Denno, 2006; Snyder et al., 2006; Schmitz, 2007). We
lack the field studies needed for a quantitative review of
the interactive effects of multiple EPN species, or of the
interactions among EPN and other soil-dwelling preda-
tors, pathogens and competitors (all factors which
could diminish potential EPN effects on hosts and
dampen trophic cascades) while also measuring im-
pacts on primary producers. Thus, we now explore what
characteristics of soil ecosystems might contribute to
variation in the strength of EPN-induced trophic cas-
cades and highlight areas of research needed to under-
stand these complex food-web interactions.
Antagonistic interactions involving EPN and the likelihood
for trophic cascades
A diverse array of organisms in multiple trophic lev-
els can influence the abundance and distribution of
EPN in soil communities (Stuart et al., 2006) and thus
their potential to kill hosts and initiate trophic cas-
cades. From the perspective of an EPN, a broad range
of host and non-host arthropods, competitors, preda-
tors and pathogens can influence their survival (Epsky
et al., 1988; Sayre and Walter, 1991; Timper et al., 1991;
Koppenh?fer et al., 1996; Kaya, 2002; Stuart et al., 2006;
Karagoz et al., 2007). However, specific interactions
among these component players are poorly studied,
even though omnivory is considered widespread in soil
communities, potentially resulting in both direct and
indirect impacts on EPN (Walter, 1988; Walter et al.,
1989; de Ruiter et al., 1996; Stuart et al., 2006). In
general, omnivory is thought to dampen top-down ef-
fects on prey populations, for instance when predators
64 Journal of Nematology, Volume 40, No. 2, June 2008
consume one another in addition to their shared prey
(Fagan, 1997; Finke and Denno, 2003).
The abundance of nematophagous fungi, bacteria,
protozoa, predaceous nematodes, mites, collembolans
and other micro-arthropods in the soil, and the high
rates of mortality they can impose in the laboratory,
suggests that these consumers might generate signifi-
cant negative impacts on EPN populations in the field
TABLE 1. Summary of studies, EPN species added, affected insect host species and plants, and log response ratios (LRR) of effect sizes.
In cases where multiple studies are used from single reports, the notes column defines the reason for treating them as independent estimates.
Publication EPN Insect host Host LRR Plant Plant LRR Notes
Belari and Boivin, 1995 S. carpocapsae Listronotus oregonensis (Coleoptera:
Curculionidae)
?1.133 carrot 0.898 1989 experiment
Belair and Boivin, 1995 S. carpocapsae Listronotus oregonensis (Coleoptera:
Curculionidae)
?0.693 carrot 0.209 1990 experiment
Canhilal and Carner,
2006
S. carpocapsae,
Heterorhabditis sp.
Melittia cucurbitae (Lepidoptera:
Sesiidae)
NR squash 0.989 1997 Trial 1
Canhilal and Carner,
2006
S. carpocapsae,
Heterorhabditis sp.
Melittia cucurbitae (Lepidoptera:
Sesiidae)
NR squash 0.924 1997 Trial 2
Canhilal and Carner,
2006
S. carpocapsae,
Heterorhabidits sp.
Melittia cucurbitae (Lepidoptera:
Sesiidae)
NR squash 0.555 1997 Trial 3
Canhilal and Carner,
2006
S. carpocapsae,
S. feltiae
Melittia cucurbitae (Lepidoptera:
Sesiidae)
NR squash 1.556 1998 Trial 1
Canhilal and Carner,
2006
S. riobrave,
S. feltiae
Melittia cucurbitae (Lepidoptera:
Sesiidae)
NR squash 1.423 1998 Trial 2
Canhilal and Carner,
2006
S. riobrave,
S. feltiae
Melittia cucurbitae (Lepidoptera:
Sesiidae)
?1.869 squash 1.258 1999 Trial 1
Canhilal and Carner,
2006
S. riobrave Melittia cucurbitae (Lepidoptera:
Sesiidae)
?0.511 squash 1.057 1999 Trial 2
Capinera et al., 1988 S. feltiae Agrotis ipsilon (Lepidoptera:
Noctuidae)
NR corn 0.614 ?
Cottrell and
Shapiro-Ilan, 2006
S. riobrave,
S. carpocapsae
Synanthedon exitiosa (Lepidoptera:
Sesiidae)
NR peach 1.085 ?
Glazer and
Goldberg, 1993
H. bacteriophora Maladera matrida (Coleoptera:
Scarabaeidae)
?0.589 peanut 0.539 1989 experiment
Glazer and
Goldberg, 1993
S. carpocapsae Maladera matrida (Coleoptera:
Scarabaeidae)
?0.673 peanut 0.762 1991 experiment
Grewal et al., 1993 S. feltiae Lycoriella mali (Diptera: Sciaridae) ?2.797 mushroom 0.033 ?
Grewal and
Richardson, 1993
S. feltiae Lycoriella auripila (Diptera:
Sciaridae)
?1.977 mushroom 0.0160 ?
Legaspi et al., 2000 S. riobrave Eoreuma loftini (Lepidoptera:
Pyralidae)
0.838 sugarcane ?0.387 ?
Levine and
Oloumi-Sadeghi, 1992
S. carpocapsae Agrotis ipsilon (Lepidoptera:
Noctuidae)
NR corn 1.197 ?
Loya and Hower, 2002 H. bacteriophora Sitona hispidulus (Coleoptera:
Curculionidae)
?1.417 alfalfa 0.237 ?
Miklasiewicz et al., 2002 S. carpocapsae,
H. bacteriophora
Listronotus oregonensis (Coleoptera:
Curculionidae)
0.234 parsley 0.032 ?
Morse and Lindegren,
1996
S. carpocapsae Asynonychus godmani (Coleoptera:
Curculionidae)
?1.535 orange 0.817 ?
Mra?c?ek et al., 1993 S. feltiae Otiorrhynchus sulcatus (Coleoptera:
Curculionidae)
NR rhododendron 0.950 ?
Parkman et al., 1994 S. scapterisci Scapteriscus sp. (Orthoptera:
Gryllotalpidae)
?0.403 grass (golf course) 0.484 ?
Preisser, 2003 H. marelatus Hepialus californicus (Lepidoptera:
Hepialidae)
?0.656 bush lupine 0.395 ?
Preisser and Strong,
2004
H. marelatus Hepialus californicus (Lepidoptera:
Hepialidae)
?0.128 bush lupine 0.199 ?
Schroeder et al., 1996 S. feltiae, S. riobrave,
H. bacteriophora,
S. carpocapsae
Delia radicum (Diptera: Anthomyiidae) ?0.267 cabbage 0.139 Trial 1 greenhouse
Schroeder et al., 1996 S. carpocapsae,
H. bacteriophora,
S. feltiae
Delia radicum (Diptera: Anthomyiidae) ?0.884 cabbage 0.243 Trial 2 greenhouse
Schroeder et al., 1996 S. feltiae Delia radicum (Diptera: Anthomyiidae) ?3.044 cabbage 0.467 Trial 3 greenhouse
Schroeder et al., 1996 S. feltiae Delia radicum (Diptera: Anthomyiidae) NR cabbage 0.450 Field experiment
Shapiro et al., 1999 S. carpocapsae Agrotis ipsilon (Lepidoptera: Noctuidae) NR corn 2.063 ?
Shields et al., 1999 H. bacteriophora Otiorhynchus ligustici (Coleoptera:
Curculionidae)
?1.807 alfalfa 0.844 ?
Strong et al., 1999 H. marelatus Hepialus californicus (Lepidoptera:
Hepialidae)
NR bush lupine 0.241 ?
Va?nninen et al., 1999 S. feltiae Delia radicum (Diptera: Anthomyiidae) ?0.146 cabbage 0.199 1987 experiment
Va?nninen et al., 1999 S. feltiae Delia radicum (Diptera: Anthomyiidae) NR cabbage 0.012 1990 experiment
West and Vrain, 1997 S. feltiae,
S. carpocapsae
Actebia fennica (Lepidoptera:
Noctuidae)
?2.0123 black spruce 1.899 1993 experiment
West and Vrain, 1997 S. feltiae,
S. carpocapsae
Actebia fennica (Lepidoptera:
Noctuidae)
?0.453 black spruce 0.398 1994 experiment
Cascading Effects of EPN Additions: Denno et al. 65
(Epsky et al., 1988; Gilmore and Potter, 1993; Kaya and
Koppenh?fer, 1996; Stuart et al., 2006). However, there
are surprisingly few manipulative studies involving EPN
and their predators and pathogens in the field. In one
experiment, infective juveniles placed in sterilized soil
survive better than in ?raw soil,? suggesting that preda-
tors and pathogens in non-treated soil adversely affect
EPN survival (Timper et al., 1991; Kaya and Koppen-
h?fer, 1996). However, determining which specific an-
tagonists are responsible for reducing EPN density has
proved challenging in a field setting.
Mites and collembolans can consume Steinernema and
Heterorhabditis species in simple laboratory microcosms,
an effect which relaxes EPN-inflicted mortality on hosts
(Gilmore and Potter, 1993; Kaya and Koppenh?fer,
1996). However, in more complex-structured meso-
cosms with turf grass added, the collembolan Folsomia
candida did not reduce the ability of Steinernema glaseri
to kill larvae of the Japanese beetle, Popillia japonica.
This study highlights how the structural complexity of
the habitat can provide spatial refuges from predation
and enhance overall top-down effects on hosts, a phe-
nomenon shown in aboveground systems (Denno and
Finke, 2006; Finke and Denno, 2006).
Nematophagous fungi, including nematode-trapping
fungi and endoparasitic fungi, are among the best-
studied natural enemies of EPN (Gray, 1988). Such
fungi can kill EPN species in simple laboratory micro-
cosms (Timper and Kaya, 1992; Kaya and Koppenh?fer,
1996; Karagoz et al., 2007). For example, nematode-
trapping fungi protected mole crickets (Scapteriscus
borellii) from infection by the EPN Steinernema feltiae in
laboratory trials (Fowler and Garcia, 1989). However,
even strong numerical responses of nematode-trapping
fungi can be ineffective at suppressing the enormous
numbers of EPN juveniles emerging from infected
hosts (Jaffee and Strong, 2005; Jaffee et al., 2007). Thus,
the explosive emergence of EPN from host cadavers
FIG. 1. Log response ratio effect sizes for EPN treatments on (A)
host insect and (B) plant response categories. Effect sizes are pre-
sented as means (?SE) across independent studies that measure vari-
ables within the same response category, with sample sizes given
above the top margin for each value. Averages across studies are
presented with filled symbols (sample sizes do not sum because some
studies reported multiple response categories). Asterisks denote ef-
fects that were adjusted (multiplied by -1) for the negative expecta-
tion for those variables (e.g., mortality expectation adjusted to same
sign as survival). The dashed line shows the null hypothesis of no
effect.
FIG. 2. Relationship between plant and host log response ratios
(LRR) in EPN-addition studies in which both effects were reported.
The signs of LRR with negative expectation (e.g., plant damage) were
adjusted by multiplying each LRR by (?1). The solid line is the best fit
linear regression (LRR
host
= ?0.27?1.11[LRR
plant
], R
2
= 0.39, df = 18,
p = 0.003), and the dashed lines show the null hypothesis of no
effect.
66 Journal of Nematology, Volume 40, No. 2, June 2008
can swamp soil-dwelling predators and destabilize
predator-prey interactions. Clearly, the conditions that
promote EPN control by nematophagous fungi and
other enemies are in need of more study (Kaya and
Koppenh?fer, 1996).
Intraguild predation (sensu Polis et al., 1989),
whereby one predator species (intraguild predator)
consumes another (intraguild prey), can severely relax
predation pressure on shared prey or host species at
lower trophic levels and dampen trophic cascades
(Schmitz et al., 2000; Halaj and Wise, 2001; Finke and
Denno, 2004; Gruner, 2004; Finke and Denno, 2006).
Such intraguild interactions involving EPN are poorly
studied, but may prove to be a significant source of
antagonism (Kaya and Koppenh?fer, 1996). For in-
stance, protozoan parasites (microsporidians in the
genera Pleistophora and Nosema) are pathogenic to both
EPN and their hosts (Veremchuk and Issi, 1970). In this
case of intraguild predation, however, it is not known if
infected EPN (intraguild prey) are less pathogenic to
their hosts.
Intraguild predation also occurs between the EPN
Steinernema carpocapsae and the parasitic wasp Diglyphus
begini, both of which attack larvae of the leafmining fly
Liriomyza trifolii on chrysanthemums (Sher et al., 2000).
Specifically, the EPN infects the host fly but also infects
larvae of D. begini, and the presence of nematodes in
mines decreases the chance of wasp survival to adult-
hood. Nonetheless, using both the parasitoid and EPN
together results in greater overall mortality on leafmin-
ers than either agent inflicts alone, in part because the
parasitoid avoids EPN-infected hosts for oviposition.
The occurrence of intraguild predation and interfer-
ence among biological control agents has generated
controversy over whether better pest suppression is
achieved by one or multiple natural enemies (Rosen-
heim, 1998; Denoth et al., 2002; Snyder et al., 2006). In
the above case involving S. carpocapsae and the para-
sitoid D. begini, intraguild predation was insufficient to
reduce survival of their shared leafminer host. Simi-
larly, the use of Heterorhabditis marelatus to suppress
Colorado potato beetle larvae had no effect on the
parasitism rate or emergence of the common larval
parasitoid Myiopharus doryphorae from beetle larvae
(Armer et al., 2004). Both of these examples suggest
that EPN and insect parasitoids complement one an-
other to suppress their host in additive fashion. As a
cautionary note, both examples involve interactions be-
tween EPN and insect parasitoids in the aboveground
food web and should not be taken as representative of
the potential for intraguild predation in the below-
ground soil community, especially between EPN and
pathogens.
Two or more EPN species often occur sympatrically,
commonly infect the same host individual, and thus
have the potential to compete interspecifically for a
shared host resource and adversely influence each oth-
er?s survival (Kaya and Koppenh?fer, 1996; Stuart et al.,
2006). The possibility for exploitative competition be-
tween two EPN is enhanced because there is little evi-
dence that infective juvenile EPN avoid hosts previously
infected by another genus or species of EPN (Lewis et
al., 2006). In the laboratory, both intra-specific and in-
ter-specific competition reduces EPN juvenile produc-
tion, and inter-specific competition can cause local ex-
tinction of a nematode species (Alatorre-Rosas and
Kaya, 1990; Kaya and Koppenh?fer, 1996). For ex-
ample, in co-infected laboratory hosts, steinernematids
usually exclude heterorhabditids, although the com-
petitive outcome depends on inoculum size, coloniza-
tion ratio and relative development rate. Studies of
inter-specific competition between steinernematid
species show that two species can co-infect a host
individual, but that one EPN species will ultimately pre-
vail to reproduction (Alatorre-Rosas and Kaya, 1990;
Kaya and Koppenh?fer, 1996). However, multiple spe-
cies can coexist in an environment if they possess dif-
ferent foraging strategies (e.g., ambushers vs. cruisers,
Lewis et al., 2006), exhibit different levels of host speci-
ficity, exploit different spatial niches in the soil, or oc-
cur in aggregated distributions (Kaya and Koppen-
h?fer, 1996; Gruner et al. unpubl. data). Such species-
specific differences in behavior and foraging niche may
explain why various combinations of EPN species result
in additive mortality of scarab beetle larvae (Choo et al.,
1996; Koppenh?fer et al., 2000), suggesting weak
interspecific competition in these cases. However, free-
living bacterivorous nematodes can compete with the
entomopathogenic nematodes in the insect host ca-
daver and may be significant regulators of nematode
densities (Duncan et al., 2003a). Release of the exotic
EPN Steinernema riobrave to control the root weevil Dia-
prepes abbreviatus resulted in the partial displacement of
endemic EPN (Duncan et al., 2003b), but S. riobrave
reproduced and persisted poorly in part due to com-
petition with bacterivorous nematodes (Duncan et al.,
2003a).
Altogether, there is extensive evidence that antago-
nistic interactions involving EPN can adversely affect
their ability to suppress host populations. However, the
EPN literature, unlike that for aboveground arthropod-
based food webs (Rosenheim et al., 1995; Snyder and
Wise, 1999; Finke and Denno, 2004; Prasad and Snyder,
2004), provides too few studies to examine quan-
titatively how multiple-enemy and competitive interac-
tions might cascade to affect plant biomass or yield.
Increased production or yield, in essence, is the ulti-
mate objective of research striving for enhanced pest
control. From the limited number of suggestive studies
that exist, EPN-pathogen or EPN-predator interactions
are likely to affect the extent that top-down effects will
cascade to basal resources, at least at a local spatial
scale.
Cascading Effects of EPN Additions: Denno et al. 67
The spatial dynamics of EPN-host interactions and
trophic cascades
The ability of natural enemies to suppress prey/host
populations is intimately linked to spatial processes and
metapopulation dynamics. For example, the ability of
predators to disperse and aggregate in areas of increas-
ing prey density are considered important attributes for
effective prey suppression and biological control (Ka-
reiva, 1990; Murdoch, 1990; D?bel and Denno, 1994),
although the presence of alternate prey and intraguild
predation can certainly affect the strength of a preda-
tor?s numerical response (Lester and Harmsen, 2002).
The infective juveniles (IJ) of EPN, however, have lim-
ited dispersal ability (Kaya and Gaugler, 1993; Lewis et
al., 2006). IJ are highly susceptible to desiccation and
are dependent on critical thresholds of soil moisture
for movement and survival, which limits their effective
dispersal to wet periods and restricts their distribution
to moist refuges under plants or deeper soil strata
(Kaya and Gaugler, 1993; Preisser et al., 2006; Stuart et
al., 2006; Ram et al., 2008b). However, by hitching rides
on non-host organisms (phoresy) and by using chemi-
cal cues from hosts or damaged plants to locate unin-
fected hosts, infective juveniles can extend their effec-
tive foraging ambit and colonizing ability (Lewis et al.,
1992; Rasmann et al., 2005; Eng et al. 2005; Lewis et al.,
2006).
Given their limited mobility and inability to persist
locally due to desiccation and other factors, it is not
surprising that EPN populations are patchy in nature
and likely exist as metapopulations (Stuart and
Gaugler, 1994; Wilson et al., 2003; Stuart et al., 2006).
In natural systems, EPN populations expand and re-
tract to spatial refuges depending on soil moisture and
host availability (Stuart et al., 2006; Ram et al., 2008b).
Although the patchiness and metapopulation structure
of EPN populations can promote the long-term persis-
tence and stability of EPN-host interactions, this spatial
structure often restricts the occurrence of strong top-
down control and EPN-driven trophic cascades in natu-
ral systems to local foci (Ram et al., 2008b). The fre-
quent decoupling of EPN-host interactions due to lim-
ited dispersal ability, local extinctions, dramatic
fluctuations in host density and a spatially constrained
numerical response likely combine to explain the lim-
ited success of EPN in providing persistent biological
control (Georgis et al., 2006).
Despite the inherent life-history constraints of EPN
and the restricted occurrence of EPN-promoted tro-
phic cascades in natural systems, our survey and meta-
analyses identified numerous cases of EPN-induced tro-
phic cascades in agricultural systems. Agricultural sys-
tems can be manipulated and thus provide the
opportunity to achieve broad-scale pest suppression
and enhanced crop yield using augmentative EPN re-
leases or conservation biological control. Management
of soil moisture and structure (e.g., porosity and or-
ganic content) to favor EPN survival and long-term per-
sistence is certainly possible. Moreover, minimizing soil
disturbance via reduced tilling may foster the conser-
vation and persistence of some EPN by preserving im-
portant spatial refuges in the soil (Lewis et al., 1998;
Stuart et al., 2006). Coupled with their high reproduc-
tive potential, advances in EPN production and delivery
methods and soil management practices may further
increase the effectiveness of EPN in promoting trophic
cascades in cropping systems (Georgis et al., 2006). Be-
cause discrepant dispersal abilities between predators
(e.g., EPN) and their prey often lead to weak numerical
responses and prey/host escape (D?bel and Denno,
1994), the appropriate timing of EPN releases could
offset their inherent dispersal limitation and improve
pest control (Georgis et al., 2006). Moreover, by select-
ing EPN species with foraging strategies that improve
host tracking, better biological control might be
achieved (Gaugler, 1999).
An improved understanding of how EPN interact
with resident natural enemies in the soil food web to
affect pest suppression is needed in the context of
large-scale ecosystems. Because multiple-enemy interac-
tions can relax top-down control and dampen trophic
cascades, it becomes critical to assess how EPN and
their associated soil-dwelling consumers (predators,
pathogens and competitors) interact. Thus, determin-
ing which combinations of consumers provide comple-
mentary control and which combinations engage in in-
traguild predation or compete becomes essential infor-
mation for improved pest management. Moreover,
there is increasing awareness that strong linkages exist
between aboveground and belowground food webs
(Wardle, 2002; Wardle et al., 2004; Kaplan et al., in
press), thereby increasing the complexity of multi-
trophic interactions. For example, when young maize
plants are infested with either the foliar lepidopteran
Spodoptera littoralis or the root-feeding beetle Diabrotica
virgifera, the parasitic wasp Cotesia marginiventris and the
entomopathogenic soil nematode Heterorhabditis megidis
are strongly attracted to their respective hosts (Ras-
mann and Turlings, 2007). However, attraction is sig-
nificantly reduced if both herbivores feed simulta-
neously on the maize plant. Notably, the emission of
the principal root attractant is reduced during double
infestation. This example suggests that via plant media-
tion, players in the aboveground community can influ-
ence the strength of EPN-host interactions in the soil.
Prospectus and synthesis
Although we lack the experimental EPN studies to
assess the effects of multiple-enemy interactions on tro-
phic cascades, one could make a tentative argument
that, even though omnivory is rampant in soil systems
(Walter et al., 1989; de Ruiter et al., 1996; Stuart et al.,
2006), we can hypothesize the effects of EPN on prey
68 Journal of Nematology, Volume 40, No. 2, June 2008
and basal resources in a three trophic-level framework.
We found evidence that EPN augmentation results in
prey suppression, reduced plant damage and positive
effects on plant yield and survival. Several factors likely
contribute to this pattern.
First, although EPN are limited in their ability to
move on their own power, they have a tremendous re-
productive potential and often outstrip any numerical
response of natural enemies (Jaffee and Strong, 2005;
Jaffee et al., 2007). Moreover, large and well-timed aug-
mentative releases of EPN in agricultural systems are
likely to temporarily swamp any potential adverse ef-
fects natural enemies on EPN. Second, the majority of
interactions among EPN individuals and species take
place within their infected and shared host (Lewis et
al., 2006), and, after colonization, intraguild predation
is less prevalent (but see Veremchuk and Issi, 1970).
Thus, EPN life history may reduce exposure to other
natural enemies compared to arthropod predators that
are exposed to top predators for a significant portion of
their immature development. However, after coloniz-
ing the same host individual, EPN are more likely to
engage in resource competition, both intraspecific and
interspecific (Stuart et al., 2006). As management tech-
niques that promote the long-term persistence of EPN
are improved, antagonistic interactions among species
and with other food web components are more likely to
arise. This probability should spur researchers to con-
duct field experiments designed to evaluate the multi-
tude of factors that dampen the strength of trophic
cascades in belowground predator-prey interactions.
LITERATURE CITED
Alatorre-Rosas, R., and Kaya, H. K. 1990. Interspecific competition
between entomopathogenic nematodes in the genera Heterorhabditis
and Steinernema for an insect host in sand. Journal of Invertebrate
Pathology 55:179?188.
Armer, C. A., Berry, R. E., Reed, G. L., and Jepsen, S. J. 2004.
Colorado potato beetle control by application of the entomopatho-
genic nematode Heterorhabditis marelata and potato plant alkaloid ma-
nipulation. Entomologia Experimentalis et Applicata 111:47?58.
Barbercheck, M. E., and Kaya, H. K. 1991. Competitive interactions
between entomopathogenic nematodes and Beauveria bassiana (Deu-
teromycotina: Hyphomycetes) in soilborne larvae of Spodoptera exigua
(Lepidoptera: Noctuidae). Environmental Entomology 20:707?712.
Belair, G., and Boivin, G. 1995. Evaluation of Steinernema carpocapsae
Weiser for control of carrot weevil adults, Listronotus oregonensis
(Leconte) (Coleoptera: Curculionidae), in organically grown carrots.
Biocontrol Science and Technology 5:225?231.
Borer, E. T., Seabloom, E. W., Shurin, J. B., Anderson, K. E., Blan-
chette, C. A., Broitman, B., Cooper, S. D., and Halpern, B. S. 2005.
What determines the strength of a trophic cascade? Ecology 86:528?
537.
Canhilal, R., and Carner, G. R. 2006. Efficacy of entomopathogenic
nematodes (Rhabditida: Steinernematidae and Heterorhabditidae)
against the squash vine borer, Melittia cucurbitae (Lepidoptera: Sesii-
dae) in South Carolina. Journal of Agricultural and Urban Entomol-
ogy 23:27?39.
Capinera, J. L., Pelissier, D., Menout, G. S., and Epsky, N. D. 1988.
Control of black cutworm, Agrotis ipsilon (Lepidoptera: Noctuidae),
with entomogenous nematodes (Nematoda: Steinernematidae, Het-
erorhabditidae). Journal of Invertebrate Pathology 52:427?435.
Cardinale, B. J., Harvey, C. T., Gross, K. L., and Ives, A. R. 2003.
Biodiversity and biocontrol: Emergent impacts of a multi-enemy as-
semblage on pest suppression and crop yield in an agroecosystem.
Ecology Letters 6:857?865.
Carpenter, S. R., and Kitchell, J. F. 1993. The trophic cascade in
lakes. New York: Cambridge University Press.
Casula, P., Wilby, A., and Thomas, M. B. 2006. Understanding
biodiversity effects on prey in multi-enemy systems. Ecology Letters
9:995?1004.
Chalcraft, D. R., and Resetarits, W. J., Jr. 2003. Predator identity
and ecological impacts: Functional redundancy or functional diver-
sity? Ecology 84:2407?2418.
Chang, G. C. 1996. Comparison of single versus multiple species of
generalist predators for biological control. Environmental Entomol-
ogy 25:207?212.
Choo, H. Y., Koppenhofer, A. M., and Kaya, H. K. 1996. Combina-
tion of two entomopathogenic nematode species for suppression of
an insect pest. Journal of Economic Entomology 89:97?103.
Cottrell, T. E., and Shapiro-Ilan, D. I. 2006. Susceptbility of the
peachtree borer, Synanthedon exitiosa,toSteinernema carpocapsae and
Steinernema riobrave in laboratory and field trials. Journal of Inverte-
brate Pathology 92:73?76.
de Ruiter, P. C., Neutel, A. M., and Moore, J. C. 1996. Energetics
and stability in belowground food webs. Pp. 201?210 in G. A. Polis
and K. O. Winemiller, eds. Food webs: Integration of patterns and
dynamics. New York: Chapman and Hall.
DeBach, P., and Rosen, D. 1991. Biological control by natural en-
emies. Cambridge, UK: Cambridge University Press.
Denno, R. F., and Finke, D. L. 2006. Multiple predator interactions
and food-web connectance: Implications for biological control. Pp.
45?70 in J. Brodeur and G. Boivin, eds. Trophic and guild interac-
tions in biological control. Dordrecht, Netherlands: Springer.
Denoth, M., Frid, L., and Myers, J. H. 2002. Multiple agents in
biological control: Improving the odds? Biological Control 24:20?30.
D?bel, H. G., and Denno, R. F. 1994. Predator-planthopper inter-
actions. Pp. 325?399 in R. F. Denno and T. J. Perfect, eds. Planthop-
pers: Their ecology and management. New York: Chapman and Hall.
Duncan, L. W., Dunn, D. C., Bague, G., and Nguyen, K. 2003a.
Competition between entomopathogenic and free-living bactivorous
nematodes in larvae of the weevil Diaprepes abbreviatus. Journal of
Nematology 35:187?193.
Duncan, L. W., Graham, J. H., Zellers, J., McCoy, C. W., and
Nguyen, K. 2003b. Incidence of endemic entomopathogenic nema-
todes following application of Steinerema riobrave for control of Dia-
prepes abbreviatus. Journal of Nematology 35:178?186.
Eng, M. S., Preisser, E. L., and Strong, D. R. 2005. Phoresy of the
entomopathogenic nematode Heterorhabditis marelatus by a non-host
organism, the isopod Porcellio scaber. Journal of Invertebrate Pathol-
ogy 88:173?176.
Epsky, N. D., Walter, D. E., and Capinera, J. L. 1988. Potential role
of nematophagous microarthropods as biotic mortality factors of en-
tomogenous nematodes (Rhabditida: Steinernematidae, Heterorhab-
ditidae). Journal of Economic Entomology 81:821?825.
Fagan, W. F. 1997. Omnivory as a stabilizing feature of natural
communities. American Naturalist 150:554?567.
Finke, D. L., and Denno, R. F. 2002. Intraguild predation dimin-
ished in complex-structured vegetation: Implications for prey sup-
pression. Ecology 83:643?652.
Finke, D. L., and Denno, R. F. 2003. Intra-guild predation relaxes
natural enemy impacts on herbivore populations. Ecological Ento-
mology 28:67?73.
Finke, D. L., and Denno, R. F. 2004. Predator diversity dampens
trophic cascades. Nature 429:407?410.
Finke, D. L., and Denno, R. F. 2005. Predator diversity and the
functioning of ecosystems: The role of intraguild predation in damp-
ening trophic cascades. Ecology Letters 8:1299?1306.
Finke, D. L., and Denno, R. F. 2006. Spatial refuge from intraguild
predation: Implications for prey suppression and trophic cascades.
Oecologia 149:265?275.
Fowler, H. G., and Garcia, C. R. 1989. Parasite-dependent proto-
cooperation. Naturwissenschaften 76:26?27.
Cascading Effects of EPN Additions: Denno et al. 69
Gaugler, R. 1999. Matching nematode and insect to achieve opti-
mal field performance. Pp. 9?14 in S. Polavarapu, ed. Optimal use of
insecticidal nematodes in pest management. New Brunswick, NJ: Rut-
gers University Press.
Georgis, R., Koppenh?fer, A. M., Lacey, L. A., B?lair, G., Duncan,
L. W., Grewal, P. S., Samish, M., Tan, L., Torr, P., and Van Tol,
R. W. H. M. 2006. Successes and failures in the use of parasitic nema-
todes for pest control. Biological Control 38:103?123.
Gilmore, S. K., and Potter, D. A. 1993. Potential role of Collembola
as biotic mortality agents for entomopathogenic nematodes. Pedo-
biologia 37:30?38.
Glazer, I., and Golberg, A. 1993. Field efficacy of entomopatho-
genic nematodes against the beetle Maladera matrida (Coleoptera:
Scarabaeidae). Biocontrol Science and Technology 3:367?376.
Gray, N. F. 1988. Fungi attacking vermiform nematodes. Pp. 3?38
in G. O. Poinar, Jr., and H. B. Jansson, eds. Diseases of nematodes.
Boca Raton, FL: CRC Press.
Grewal, P. S., and Richardson, P. N. 1993. Effects of application
rates of Steinernema feltiae (Nematoda: Steinernematidae) on biologi-
cal control of the mushroom fly Lycoriella auripila (Diptera: Sciari-
dae). Biocontrol Science and Technology 3:29?40.
Grewal, P. S., Tomalak, M., Keil, C. B. O., and Gaugler, R. 1993.
Evaluation of a genetically selected strain of Steinernema feltiae against
the mushroom sciarid Lycoriella mali. Annals of Applied Biology 123:
695?702.
Gruner, D. S. 2004. Attenuation of top-down and bottom-up forces
in a complex terrestrial community. Ecology 85:3010?3022.
Gruner, D. S., Ram, K., and Strong, D. R. 2007. Soil mediates the
interaction of coexisting entomopathogenic nematodes with an in-
sect host. Journal of Invertebrate Pathology 94:12?19.
Gurevitch, J., and Hedges, L. V. 1999. Statistical issues in ecological
meta-analyses. Ecology 80:1142?1149.
Gurr, G. M., Wratten, S. D., and Altieri, M. A. 2004. Ecological
engineering for pest management: Advances in habitat manipulation
for arthropods. Collingwood, Australia: CSIRO Publishing.
Halaj, J., and Wise, D. H. 2001. Terrestrial trophic cascades: How
much do they trickle? American Naturalist 157:262?281.
Hedges, L. V., Gurevitch, J., and Curtis, P. S. 1999. The meta-
analysis of response ratios in experimental ecology. Ecology 80:1150?
1156.
Heinz, K. M., and Nelson, J. M. 1996. Interspecific interactions
among natural enemies of Bemisia in an inundative biological control
program. Biological Control 6:384?393.
Hochberg, M. E. 1996. Consequences for host population levels of
increasing natural enemy species richness in classical biological con-
trol. American Naturalist 147:307?318.
Jaffee, B., Bastow, J., and Strong, D. 2007. Suppression of nema-
todes in a coastal grassland soil. Biology and Fertility of Soils 44:19?
26.
Jaffee, B. A., and Strong, D. R. 2005. Strong bottom-up and weak
top-down effects in soil: Nematode-parasitized insects and nematode-
trapping fungi. Soil Biology and Biochemistry 37:1011?1021.
Kaplan, I., Sardanelli, S., and Denno, R. F. In press. Field evidence
for indirect interactions between foliar-feeding insect and root-
feeding nematode communities on Nicotiana tabacum. Ecological
Entomology.
Karagoz, M., Gulcu, B., Cakmak, I., Kaya, H., and Hazir, S. 2007.
Predation of entomopathogenic nematodes by Sancassania sp. (Acari:
Acaridae). Experimental and Applied Acarology 43:85?95.
Kareiva, P. 1990. Population dynamics in spatially complex envi-
ronments: Theory and data. Philosophical Transactions of the Royal
Society of London-B 330:175?190.
Kaya, H. K. 2002. Natural enemies and other antagonists. Pp. 189?
204 in R. Gaugler, ed. Entomopathogenic nematology. London:
CABI Publishing.
Kaya, H. K., and Gaugler, R. 1993. Entomopathogenic nematodes.
Annual Review of Entomology 38:181?206.
Kaya, H. K., and Koppenh?fer, A. M. 1996. Effects of microbial and
other antagonistic organism and competition on entomopathogenic
nematodes. Biocontrol Science and Technology 6:357?371.
Koppenh?fer, A. M., Jaffee, B. A., Muldoon, A. E., Strong, D. R.,
and Kaya, H. K. 1996. Effect of nematode-trapping fungi on an en-
tomopathogenic nematode originating from the same field site in
California. Journal of Invertebrate Pathology 68:246?252.
Koppenh?fer, A. M., Wilson, M., Brown, I., Kaya, H. K., and
Gaugler, R. 2000. Biological control agents for white grubs (Coleop-
tera: Scarabaeidae) in anticipation of the establishment of the Japa-
nese beetle in California. Journal of Economic Entomology 93:71?80.
Lajeunesse, M. J., and Forbes, M. R. 2003. Variable reporting and
quantitative reviews: A comparison of three meta-analytical tech-
niques. Ecology Letters 6:448?454.
Landis, D., Wratten, S. D., and Gurr, G. M. 2000. Habitat manage-
ment to conserve natural enemies of arthropod pests in agriculture.
Annual Review of Entomology 45:175?201.
Legaspi, J. C., Legaspi, B. C., and Saldana, R. R. 2000. Evaluation of
Steinernema riobravis (Nematoda: Steinernematidae) against the Mexi-
can rice borer (Lepidoptera: Pyralidae). Journal of Entomological
Science 35:141?149.
Lester, P. J., and Harmsen, R. 2002. Functional and numerical
responses do not always indicate the most effective predator for bio-
logical control: An analysis of two predators in a two-prey system.
Journal of Applied Ecology 39:455?468.
Levine, E., and Oloumi-Sadeghi, H. 1992. Field evaluation of Stein-
ernema carpocapsae (Rhabditida, Steinernematidae) against black cut-
worm (Lepidoptera: Noctuidae) larvae in field corn. Journal of En-
tomological Science 27:427?435.
Lewis, E. E., Campbell, J. F., and Gaugler, R. 1998. A conservation
approach to using entomopathogenic nematodes in turf and land-
scapes. Pp. 235?254 in P. Barbosa, ed. Conservation biological con-
trol. London: Academic Press.
Lewis, E. E., Campbell, J., Griffin, C., Kaya, H., and Peters, A. 2006.
Behavioral ecology of entomopathogenic nematodes. Biological Con-
trol 38:66?79.
Lewis, E. E., Gaugler, R., and Harrison, R. 1992. Entomopatho-
genic nematode host finding: Response to host contact cues by cruise
and ambush foragers. Parasitology 105:309?315.
Losey, J. E., and Denno, R. F. 1998. Interspecific variation in the
escape responses of aphids: Effect on risk of predation from foliar-
foraging and ground-foraging predators. Oecologia 115:245?252.
Loya, L. J., and Hower, A. A., Jr. 2002. Population dynamics, per-
sistence, and efficacy of the entomopathogenic nematode Heterorhab-
ditis bacteriophora (Oswego strain) in association with the clover root
curculio (Coleoptera: Curculionidae) in Pennsylvania. Environmen-
tal Entomology 31:1240?1250.
Miklasiewicz, T. J., Grewal, P. S., Hoy, C. W., and Malik, V. S. 2002.
Evaluation of entomopathogenic nematodes for suppression of car-
rot weevil. BioControl 47:545?561.
Mikola, J., and Set?l?, H. 1998. No evidence of trophic cascades in
an experimental microbial-based soil food web. Ecology 79:153?164.
Morse, J. G., and Lindegren, J. E. 1996. Suppression of fuller rose
beetle (Coleoptera: Curculionidae) on citrus with Steinernema carpo-
capsae (Rhabditida: Steinernematidae). Florida Entomologist 79:373?
384.
Mr?c?ek, Z. 2002. Use of entomoparasitic nematodes (EPANs) in
biological control. Pp. 235?264 in R. K. Upadhyay, ed. Advances in
microbial control of insect pests. New York: Kluwer Academic.
Mr?c?ek, Z., Jiskra, K., and Kahounova, L. 1993. Efficiency of stein-
ernematid nematodes (Nematoda: Steinernematidae) in controlling
larvae of the black vine weevil, Otiorrhynchus sulcatus (Coleoptera:
Curculionidae), in laboratory and field experiments. European Jour-
nal of Entomology 90:71?76.
Murdoch, W. W. 1990. The relevance of pest-enemy models to
biological control. Pp. 1?24 in M. Mackauer, L. E. Ehler, and J. Ro-
land, eds. Critical issues in biological control. Andover, UK: Inter-
cept.
Norris, R. F., Caswell-Chen, E. P., and Kogan, M. 2003. Concepts in
integrated pest management. Upper Saddle River, NJ: Prentice Hall.
Otto, S. B., Berlow, E. L., Rank, N. E., Smiley, J., and Brose, U.
2008. Predator diversity and identity drive interaction strength and
trophic cascades in a food web. Ecology 89:134?144.
Pace, M. L., Cole, J. J., Carpenter, S. R., and Kitchell, J. F. 1999.
70 Journal of Nematology, Volume 40, No. 2, June 2008
Trophic cascades revealed in diverse ecosystems. Trends in Ecology
and Evolution 14:483?488.
Parkman, J. P., Frank, J. H., Nguyen, K. B., and Smart, G. C. 1994.
Inoculative release of Steinernema scapterisci (Rhabditida: Steinerne-
matidae) to suppress pest mole crickets (Orthoptera: Gryllotalpidae)
on golf-courses. Environmental Entomology 23:1331?1337.
Polis, G. A., Myers, C. A., and Holt, R. D. 1989. The ecology and
evolution of intraguild predation: Potential competitors that eat each
other. Annual Review of Ecology and Systematics 20:297?330.
Polis, G. A., Sears, A. L. W., Huxel, G. R., Strong, D. R., and Maron,
J. 2000. When is a trophic cascade a trophic cascade? Trends in
Ecology and Evolution 15:473?475.
Portillo-Aguilar, C., Villani, M. G., Tauber, M. J., Tauber, C. A., and
Nyrop, J. P. 1999. Entomopathogenic nematode (Rhabditida: Heter-
orhabditidae and Steinernematidae) response to soil texture and
bulk density. Environmental Entomology 28:1021?1035.
Prasad, R. P., and Snyder, W. E. 2004. Predator interference limits
fly egg biological control by a guild of ground-active beetles. Biologi-
cal Control 31:428?437.
Preisser, E. L. 2003. Field evidence for a rapidly cascading under-
ground food web. Ecology 84:869?874.
Preisser, E. L., Dugaw, C. J., Dennis, B., and Strong, D. R. 2006.
Plant facilitation of a belowground predator. Ecology 87:1116?1123.
Preisser, E. L., and Strong, D. R. 2004. Climate affects predator
control of an herbivore outbreak. American Naturalist 163:754?762.
R Development Core Team. 2008. R: a language and environment
for statistical computing. R Foundation for Statistical Computing,
Vienna, Austria. ISBN 3?900051?07?0, URL http://www.R-
project.org.
Ram, K., Gruner, D. S., McLaughlin, J. P., Preisser, E. L., and
Strong, D. R. 2008a. Dynamics of a subterranean trophic cascade in
space and time. Journal of Nematology 40:85?92.
Ram, K., Preisser, E. L., Gruner, D. S., and Strong, D. R. 2008b.
Metapopulation dynamics override local limits on long-term parasite
persistence. Ecology. In press.
Rasmann, S., K?llner, T. G., Degenhardt, J., Hiltpold, I., Toepfer,
S., Kuhlmann, U., Gershenzon, J., and Turlings, T. C. J. 2005. Re-
cruitment of entomopathogenic nematodes by insect-damaged maize
roots. Nature 434:732?737.
Rasmann, S., and Turlings, T. C. J. 2007. Simultaneous feeding by
aboveground and belowground herbivores attenuates plant-mediated
attraction of their respective natural enemies. Ecology Letters 10:
926?936.
Riechert, S. E., and Lawrence, K. 1997. Test for predation effects of
single versus multiple species of generalist predators: Spiders and
their insect prey. Entomologia Experimentalis et Applicata 84:147?
155.
Rosenheim, J. A. 1998. Higher-order predators and the regulation
of insect herbivore populations. Annual Review of Entomology 43:
421?447.
Rosenheim, J. A., Kaya, H. K., Ehler, L. E., Marois, J. J., and Jaffee,
B. A. 1995. Intraguild predation among biological-control agents:
Theory and evidence. Biological Control 5:303?335.
Rosenheim, J. A., Wilhoit, L. R., and Armer, C. A. 1993. Influence
of intraguild predation among generalist insect predators on the
suppression of an herbivore population. Oecologia 96:439?449.
Sasser, J. N., and Freckman, D. W. 1987. A world perspective on
nematology: The role of the society. Pp. 7?14 in J. A. Veech and D. W.
Dickson, eds. Vistas on nematology. Hyattsville, MD: Society of Nema-
tologists, Inc.
Sayre, R. M., and Walter, D. E. 1991. Factors affecting the efficacy
of natural enemies of nematodes. Annual Review of Phytopathology
29:149?166.
Schmitz, O. J. 2007. Predator diversity and trophic interactions.
Ecology 88:2415?2426.
Schmitz, O. J., Beckerman, A. P., and O?Brien, K. M. 1997. Behav-
iorally mediated trophic cascades: Effects of predation risk on food
web interactions. Ecology 78:1388?1399.
Schmitz, O. J., Hamb?ck, P. A., and Beckerman, A. P. 2000. Tro-
phic cascades in terrestrial systems: A review of the effects of carnivore
removals on plants. American Naturalist 155:141?153.
Schroeder, P. C., Ferguson, C. S., Shelton, A. M., Wilsey, W. T.,
Hoffmann, M. P., and Petzoldt, C. 1996. Greenhouse and field evalu-
ations of entomopathogenic nematodes (Nematoda: Heterorhabditi-
dae and Steinernematidae) for control of cabbage maggot (Diptera:
Anthomyiidae) on cabbage. Journal of Economic Entomology 89:
1109?1115.
Shapiro, D. I., Lewis, L. C., Obrycki, J. J., and Abbas, M. 1999.
Effects of fertilizers on suppression of black cutworm (Agrotis ipsilon)
damage with Steinernema carpocapsae. Journal of Nematology 31:690?
693.
Sher, R. B., Parrella, M. P., and Kaya, H. K. 2000. Biological control
of the leafminer Liriomyza trifolii (Burgess): Implications for intra-
guild predation between Diglyphus begini Ashmead and Steinernema
carpocapsae (Weiser). Biological Control 17:155?163.
Shields, E. J., Testa, A., Miller, J. M., and Flanders, K. L. 1999. Field
efficacy and persistence of the entomopathogenic nematodes Heter-
orhabditis bacteriophora ?Oswego? and H. bacteriophora ?NC? on alfalfa
snout beetle larvae (Coleoptera: Curculionidae). Environmental En-
tomology 28:128?136.
Shurin, J. B., Borer, E. T., Seabloom, E. W., Anderson, K., Blan-
chette, C. A., Broitman, B., Cooper, S. D., and Halpern, B. S. 2002. A
cross-ecosystem comparison of the strength of trophic cascades. Ecol-
ogy Letters 5:785?791.
Snyder, W. E., Chang, G. C., and Prasad, R. P. 2005. Conservation
biological control: Biodiversity influences the effectiveness of preda-
tors. Pp. 324?343 in P. Barbosa and I. Castellanos, eds. Ecology of
predator-prey interactions. London, UK: Oxford University Press.
Snyder, W. E., and Ives, A. R. 2001. Generalist predators disrupt
biological control by a specialist parasitoid. Ecology 82:705?716.
Snyder, W. E., Snyder, G. B., Finke, D. L., and Straub, C. S. 2006.
Predator biodiversity strengthens herbivore suppression. Ecology Let-
ters 9:789?796.
Snyder, W. E., and Wise, D. H. 1999. Predator interference and the
establishment of generalist predator populations for biocontrol. Bio-
logical Control 15:283?292.
Snyder, W. E., and Wise, D. H. 2001. Contrasting trophic cascades
generated by a community of generalist predators. Ecology 82:1571?
1583.
Sohlenius, B. 1980. Abundance, biomass and contribution to en-
ergy-flow by soil nematodes in terrestrial ecosystems. Oikos 34:186?
194.
Soluk, D. A. 1993. Multiple predator effects: Predicting combined
functional response of stream fish and invertebrate predators. Ecol-
ogy 74:219?225.
Stanton, N. L. 1988. The underground in grasslands. Annual Re-
view of Ecology and Systematics 19:573?589.
Stiling, P., and Cornelissen, T. 2005. What makes a successful bio-
control agent? A meta-analysis of biological control agent perfor-
mance. Biological Control 34:236?246.
Straub, C. S., and Snyder, W. E. 2006. Species identity dominates
the relationship between predator biodiversity and herbivore sup-
pression. Ecology 87:277?282.
Strong, D. R., Kaya, H. K., Whipple, A. L., Child, A. L., Kraig, S.,
Bondonno, M., Dyer, K., and Maron, J. L. 1996. Entomopathogenic
nematodes: Natural enemies of root-feeding caterpillars on bush lu-
pine. Oecologia 108:167?173.
Strong, D. R., Whipple, A. V., Child, A. L., and Dennis, B. 1999.
Model selection for a subterranean trophic cascade: Root-feeding
caterpillars and entomopathogenic nematodes. Ecology 80:2750?
2761.
Stuart, R. J., Barbercheck, M. E., Grewal, P. S., Taylor, R. A. J., and
Hoy, C. W. 2006. Population biology of entomopathogenic nema-
todes: Concepts, issues, and models. Biological Control 38:80?102.
Stuart, R. J., and Gaugler, R. 1994. Patchiness in populations of
entomopathogenic nematodes. Journal of Invertebrate Pathology 64:
39?45.
Symondson, W. O. C., Sunderland, K. D., and Greenstone, M. H.
2002. Can generalist predators be effective biocontrol agents? Annual
Review of Entomology 47:561?594.
Timper, P., and Kaya, H. K. 1992. Impact of a nematode-parasitic
Cascading Effects of EPN Additions: Denno et al. 71
fungus on the effectiveness of entomopathogenic nematodes. Journal
of Nematology 24:1?8.
Timper, P., Kaya, H. K., and Jaffee, B. A. 1991. Survival of ento-
mogenous nematodes in soil infested with the nematode-parasitic
fungus Hirsutella rhossiliensis (Deuteromycotina: Hyphomycetes). Bio-
logical Control 1:42?50.
V?nninen, I., Hokkanen, H., and Tyni-Juslin, J. 1999. Screening of
field performance of entomopathogenic fungi and nematodes
against cabbage root flies (Delia radicum L. and D. floralis (Fall.);
Diptera, Anthomyiidae). Acta Agriculturae Scandinavica Section B-
Soil and Plant Science 49:167?183.
Veremchuk, G. V., and Issi, I. V. 1970. The development of micro-
sporidians of insects in the entomopathogenic nematode Neoaplec-
tana agriotos (Nematoda: Steinernematidae). Parazitologiya 4:3?7.
Walter, D. E. 1988. Nematophagy by soil arthropods from the short-
grass steppe, Chihuahuan desert and Rocky Mountains of the central
United States. Agriculture, Ecosystems and Environment 24:307?316.
Walter, D. E., Moore, J. C., and Loring, S. J. 1989. Symphylella sp.
(Symphyla: Scolopendrellidae) predators of arthropods and nema-
todes in grassland soils. Pedobiologia 33:113?116.
Wardle, D. A. 2002. Communities and ecosystems: Linking the
aboveground and belowground components. Princeton, NJ: Prince-
ton University Press.
Wardle, D. A., Bardgett, R. D., Klironomos, J. N., Setala, H., van der
Putten, W. H., and Wall, D. H. 2004. Ecological linkages between
aboveground and belowground biota. Science 304:1629?1633.
Wardle, D. A., Williamson, W. H., Yeates, G. W., and Bonner, K. I.
2005. Trickle-down effects of aboveground trophic cascades on the
soil food web. Oecologia 111:348?358.
West, R. J., and Vrain, T. C. 1997. Nematode control of black army
cutworm (Lepidoptera: Noctuidae) under laboratory and field con-
ditions. Canadian Entomologist 129:229?239.
Wilby, A., Villareal, S. C., Lan, L. P., Heong, K. L., and Thomas, M.
B. 2005. Functional benefits of predator species diversity depend on
prey identity. Ecological Entomology 30:497?501.
Wilson, M. J., Lewis, E. E., Yoder, F., and Gaugler, R. 2003. Appli-
cation pattern and persistence of the entomopathogenic nematode
Heterorhabditis bacteriophora. Biological Control 26:180?188.
72 Journal of Nematology, Volume 40, No. 2, June 2008