vol. 157, no. 3
the american naturalist
march 2001
Terrestrial Trophic Cascades: How Much Do They Trickle?
Juraj Halaj* and David H. Wise†
Department of Entomology, University of Kentucky, Lexington,
Kentucky 40546-0091
Submitted February 14, 2000; Accepted October 19, 2000
abstract: Although more consensus is now emerging on the magnitude and frequency of cascading trophic effects in aquatic communities, the debate over their terrestrial counterparts continues. We
used meta-analysis to analyze field experiments on trophic cascades
in terrestrial arthropod-dominated food webs to evaluate the overall
magnitude of trophic cascades and conditions affecting their occurrence and strength. We found extensive support for the presence of
trophic cascades in terrestrial communities. In the majority of experiments, predator removal led to increased densities of herbivorous
insects and higher levels of plant damage. Cascades in which removing predators led to decreased herbivory also were detected but
were less frequent and weaker, suggesting a predominantly threetrophic-level behavior of arthropod-dominated terrestrial food webs.
Despite the clear evidence that cascades often decreased plant damage, residual effects of predation produced either no or only minimal
changes in overall plant biomass. Agricultural systems and natural
communities exhibited similarly strong effects of predation on herbivore abundance. However, resulting effects on plant damage and
community-wide effects of trophic cascades on plant biomass usually
were highly variable, and only in the managed agricultural systems
did predators occasionally have strong indirect effects on plant biomass. Our meta-analysis suggests that the effects of trophic cascades
on the biomass of primary producers are weaker in terrestrial than
aquatic food webs.
Keywords: food webs, generalist predators, herbivory, meta-analysis,
primary producers, trophic cascades.
Despite extensive theoretical and empirical work on indirect effects in ecological communities (Paine 1966; Holt
1977; Abrams 1987, 1995; Stamp and Bowers 1991; Holt
and Lawton 1993; Billick and Case 1994), the significance
of these interactions is only poorly understood (Strauss
1991; Wootton 1994; Abrams 1995; Menge 1995). One
* E-mail: [email protected].
†
Corresponding author; e-mail: [email protected].
Am. Nat. 2001. Vol. 157, pp. 262–281. q 2001 by The University of Chicago.
0003-0147/2001/15703-0002$03.00. All rights reserved.
form of indirect effect includes trophic events triggered by
predation. Direct effects of a predator (donor) on its prey
(transmitter) translate into changes in the prey’s energy
supply (receiver) in an interaction chain (sensu Wootton
1993, 1994). Effects of resource consumption thus “cascade” from top consumers to the base of the Eltonian
energy pyramid via feeding links between inversely related
trophic levels (Paine 1980; Carpenter et al. 1985).
In recent decades, the theory of trophic cascades has been
rigorously developed and tested in aquatic systems. For example, experimental studies showed that piscivorous fish
frequently reduce the abundance of planktivorous fish species. Size-dependent predation of planktivores on zooplankton assemblages (Brooks and Dodson 1965; Carpenter et
al. 1985) may consequently alter the grazing pressure on
primary producers, algal phytoplankton (Hrbácek et al.
1961; Carpenter et al. 1985; Vanni and Findlay 1990).
Trophic cascades appear to be a significant and widespread
type of indirect interaction in freshwater communities
(Power et al. 1985; Carpenter et al. 1987; Power 1990; Vanni
and Findlay 1990; Brett and Goldman 1996).
The possibility of trophic cascades in terrestrial communities has long been recognized. Early references to
cascading top-down effects date back to the Chinese, who
as early as 2,500 yr ago promoted populations of predators
to alleviate crop damage (Begon et al. 1996). In 1752,
Linnaeus pointed out the benefits of using predatory arthropods to control crop pests (NRC 1996). Nevertheless,
the actual role of trophic cascades in shaping the structure
of terrestrial systems has been debated vigorously. Proponents of “the green world hypothesis” (HSS hypothesis;
Hairston et al. 1960; Slobodkin et al. 1967) argue for the
paramount role of predation (“top-down” effects) exerting
cascading influences on the rest of the community. The
hypothesis predicts that food-limited predators suppress
herbivore populations to densities at which plants experience negligible levels of herbivory. In its original form,
the HSS hypothesis applied only to folivores and sap and
bark feeders in natural climax communities; however, its
predictions have been compared with patterns in a diversity of taxa and systems (Sih et al. 1985; Schoener 1989;
Polis 1994).
The reasoning behind the HSS hypothesis has been ex-
Terrestrial Trophic Cascades 263
trapolated to more than or fewer than three trophic levels
by incorporating effects of ecosystem productivity (EEH;
Fretwell 1977; Oksanen et al. 1981; Oksanen and Oksanen
2000). According to EEH, strong effects of herbivory
should be prevalent in both unproductive (two trophic
levels, no predators) and highly productive environments
with even numbers of trophic levels, whereas herbivores
should exert much weaker control of primary production
in moderately productive systems with odd numbers of
trophic levels. This linear trophic model assumes the presence of only one homogeneous functional group (“guild”)
at each trophic level (Oksanen et al. 1981; Oksanen and
Oksanen 2000). However, Leibold (1989) and Abrams
(1993) have shown that an increase in system heterogeneity
(e.g., more than one guild at each trophic level, feeding
of a guild across several trophic levels, or consumer’s diet
breadth) may alter responses of the trophic chain to the
input of nutrients and produce trophic effects inconsistent
with EEH predictions.
Alternatively, some argue against the prevalence of
trophic cascades in terrestrial systems. Propagation of indirect effects requires a relatively simple environment, in
which strong trophic links and recipient control operate
through a few key consumers (Paine 1980; Strong 1992),
which may rarely occur in terrestrial systems. The reticulate nature of most terrestrial food webs, intraguild predation, and widespread trophic-level omnivory imply that
terrestrial webs are strongly nonlinear trophic structures
with the potential to buffer cascading effects (Polis et al.
1989; Polis 1991; Hunter and Price 1992; Polis and Holt
1992; Strong 1992), causing an incipient trophic cascade
to become disconnected along the trophic chain (Schoener
1993; Abrams et al. 1996). Only under unusual conditions
(e.g., presence of trophic subsidies; Polis 1999) in terrestrial systems can consumers generate strong cascading effects (MacInnes and Kerbes 1987; Strong 1992; Polis 1994;
Polis and Strong 1996); thus, in most terrestrial food webs,
instead of rushing cascades, “trophic trickles” are expected
to be the norm (Strong 1992). The arguments against
strong trophic cascades thus imply a donor-controlled,
bottom-up template for terrestrial systems (White 1978;
Hunter and Price 1992; Strong 1992; Polis 1994; Polis and
Strong 1996).
It is still too early to make reliable predictions about
which communities exhibit strong cascading effects. The
occurrence and strength of trophic cascades likely vary
along a community continuum rather than being solely
based on the community’s aquatic or terrestrial quality
(Strong 1992). The simple aquatic-terrestrial dichotomy
does not always hold. Even in many aquatic trophic cascades, the residual effects of predation on phytoplankton
are usually weak (Brett and Goldman 1996, 1997), and
factors such as nutrient enrichment and recycling (Vanni
and Findlay 1990; Brett and Goldman 1997) or antagonistic interactions among zooplankton species (McCann
et al. 1998) may modify the strength of top-down control
in aquatic systems. Effects of predation cascading to primary producers have been detected in many terrestrial
systems. This is true in relatively simple systems such as
agroecosystems (Wright et al. 1960; Coaker 1965; Risch
and Carroll 1982; Riechert and Bishop 1990; Carter and
Rypstra 1995), grasslands (Schmitz 1994; Chase 1996;
Moran et al. 1996; Schmitz et al. 1997; Moran and Hurd
1998), and scrub communities (Spiller and Schoener 1990,
1994; Polis and Hurd 1996), as well as in some of the
most diverse terrestrial ecosystems, including temperate
forests (Altegrim 1989; Marquis and Whelan 1994), tropical rain forests (Dial 1992; Letourneau and Dyer 1998),
and soil communities (Strong et al. 1996a, 1996b, 1999).
Regardless of their position on the trophic-cascade argument, most terrestrial ecologists now agree that insufficient evidence precludes generalizations about the functioning of species-rich systems (Oksanen et al. 1981;
Strong 1992; Chase 1996; Letourneau and Dyer 1998; Lawton 1999; Oksanen and Oksanen 2000). Under some conditions, terrestrial communities clearly show cascading
trophic effects. But how widespread and how strong are
these effects? The focus now should be on resolving what
factors favor the occurrence and modulate the magnitude
of trophic cascades in terrestrial systems.
Meta-analysis of Terrestrial Trophic Cascades
Our objective was a quantitative assessment of the occurrence and strength of trophic cascades in terrestrial grazing
food webs. We focused our review on the grazing subsystem of terrestrial food webs as a result of a greater availability of experimental data on trophic cascades in these
systems. Cascading trophic effects in terrestrial detrital
food webs (e.g., Kajak and Jakubczyk 1977; Kajak 1997;
Lawrence and Wise 2000) is a growing area of ecological
research and warrants a future separate assessment. We
used meta-analysis to summarize our results. In contrast
to more conventional, vote-counting literature reviews,
meta-analysis allows a quantitative summary of findings
and identification of central tendencies in a collection of
different studies (Hedges and Olkin 1985; Gurevitch et al.
1992). Despite an increasing application of meta-analysis
to ecological questions (Järvinen 1991; Gurevitch et al.
1992; Tonhasca and Byrne 1994; Brett and Goldman 1996;
Hartley and Hunter 1998; Koricheva et al. 1998), its use
in ecology remains controversial. A high diversity of ecological interactions and methods of study require a cautious approach to generalization (Osenberg et al. 1999).
However, if meta-analysis is used predominantly to summarize findings and to generate new hypotheses for future
264 The American Naturalist
testing, it can be a powerful tool of research synthesis in
ecology (Gurevitch et al. 1992; Englund et al. 1999; Goldberg et al. 1999; Gurevitch and Hedges 1999; Palmer 1999).
We used meta-analysis to address a set of a priori questions: What is the overall prevalence and magnitude of
trophic cascades in terrestrial communities? Do effects vary
among different categories of primary producers? Are the
effects of trophic cascades stronger in managed than natural habitats?
The recent publication of a meta-analysis of terrestrial
trophic cascades by Schmitz et al. (2000) provides a unique
opportunity to assess the generality of findings from two
independent meta-analyses. Despite many similarities in
findings and techniques of meta-analysis, our approach
and that of Schmitz et al. (2000) differ in three major
ways: First, we included experiments in agricultural crops,
a category of studies explicitly excluded by Schmitz et al.
(2000). By including crop systems, we were able to contrast
managed and natural communities and to assess the magnitude of the trophic cascade across a sharp gradient of
producer quality and habitat complexity. Second, Schmitz
et al. (2000) included “natural” experiments in which
predator densities differed between nonmanipulated areas.
We excluded such observational studies because observed
densities of herbivores and plant responses could have
been caused by factors other than indirect effects of predation. Third, almost 60% of the tests in Schmitz et al.
(2000) had ants as manipulated predators. Although these
insect predators are a major component of terrestrial food
webs, such a high proportion of ant-centered studies may
have introduced a bias. Like Schmitz et al. (2000), we
unavoidably examined arthropod-dominated food webs
(see below), yet our data set provides a broader selection
of predators.
Methods and Analyses
Literature Search and Data Selection
Database. We broadly searched the ecological literature for
studies documenting the occurrence of trophic cascades in
natural and managed terrestrial communities using standard
publication search engines (Agricola, Biological Abstracts,
Biological and Agricultural Index, Science Citation Index).
We also extensively consulted literature lists in published
papers. To reduce unconscious bias from selective reporting
in compiling meta-analysis data sets (Englund et al. 1999;
Palmer 1999), we had no a priori criteria for the quality of
the publication source, but individual publications were critically screened (see below). We included studies performed
specifically to test the occurrence of trophic cascades (e.g.,
basic food web research literature) and also those where
trophic cascade effects were implicit from research objectives
(e.g., biocontrol research literature).
Publication Selection Criteria. We included in our analysis
only studies that satisfied the following criteria: First, the
investigation was a field experiment in which predator densities were manipulated directly, for example, by removal
or stocking, or indirectly by alteration of the habitat either
to enhance or to reduce predator numbers. Second, the
study included an appropriate control. For the purpose of
comparing studies, we designated the control to be the treatment in which predator density was closest to the natural
level in the study system (Gurevitch et al. 1992; Rosenberg
et al. 1997), which did not always correspond to the treatment identified as the control by the investigators. Thus,
predator-removal and predator-enhancement treatments
were considered experimental groups. Third, measures of
variance and number of replicates were reported or could
be obtained from the author. Finally, the study measured
cascading effects of predation on primary producers as either changes in plant damage (i.e., percentage of injury) or
plant abundance (i.e., biomass or vegetation cover). We
analyzed data on changes in herbivore densities if they were
reported. We also included studies in which the effect on
herbivores was not stated but in which it was implicit that
observed changes in plant performance resulted from altered grazing intensity by herbivores as a result of predator
manipulations.
Nonindependence. Separate experiments in one published
paper that were established consecutively over the season
or during different years were treated as independent comparisons, as were comparisons for several species (groups)
of organisms responding to the same treatment. These
criteria follow consensus in conventional (Connell 1983;
Sih et al. 1985) and meta-analytic reviews (Gurevitch et
al. 1992; Koricheva et al. 1998). In a series of treatments
in the same study, effects of the highest predator addition
and the lowest predator reduction were compared with
the same control, and these were treated as independent
comparisons. The seasonal mean for control and experimental groups was used if the response variable was measured over time; otherwise, the largest contrast between
control and experimental group was selected.
Our selection guidelines clearly resulted in sets of nonindependent comparisons. It has been argued, however,
that selective omission of some contrasts from a metaanalysis may introduce more bias than the use of a larger
set of nonindependent comparisons (Gurevitch et al.
1992). We postulated that including several comparisons
from the same study (or same author) and thus using their
average effect in the analysis provided a better assessment
of treatment effects than selecting a subset of comparisons
Terrestrial Trophic Cascades 265
based on dubious selection criteria. If several response
variables were measured to evaluate the same treatment
impact (e.g., herbivore abundance expressed as either egg,
larval, or adult densities), we selected one parameter, the
one showing the greatest effect, to lower possible nonindependent bias of including multiple responses (Gurevitch
and Hedges 1999).
Publication Bias. A large percentage of comparisons in several categories came from work of only a few authors,
which could have biased the independence of our overall
data set. To evaluate the effect of including these groups
of publications, we compared mean effect size of each
group against the mean effect size of the rest of the main
data set using the between-class homogeneity statistic Qb.
Its significance was measured with a x2 test (Gurevitch et
al. 1992; Rosenberg et al. 1997). The extent of selective
reporting was further evaluated by examining the scatter
plot of effect size and sample size (Light and Pillemer 1984;
Palmer 1999). For the purpose of this assessment, an average of sample sizes was used in experiments with unequal
sample sizes in control and experimental groups.
In addition to the standard measure of effect size (d1),
we also performed meta-analyses with response ratios
(RR). The response ratio (ratio of means of experimental
and control groups; RR p X e /X c) is a relatively new statistic to measure effect size in ecological meta-analysis.
The recent description by Hedges et al. (1999) of the
statistical properties of response ratios facilitates their
wider application in ecology. Response ratios are generally analyzed using their natural logarithms (L p
ln (RR)) to improve their statistical properties. To minimize the bias of using ln (RR) , it is recommended that
either Ïne X e /SDe or Ïnc X c /SDc, whichever is smaller,
be 13.0 (Hedges et al. 1999; X, n, and SD denote the
mean, sample size, and standard error, respectively, of
experimental, e, and control groups, c). Since over 83%
of Ïnc X c /SDc and 82% of all Ïne X e /SDe values in our
data set were 13.0, we felt confident that our database
was suitable for meta-analysis with response ratios. By
including ln (RR), we attempted to minimize the possible
bias of using a unique measure of effect size (Osenberg
et al. 1997). All meta-analyses were performed with
MetaWin statistical software (Rosenberg et al. 1997).
Statistical Analyses
Results and Discussion
We used biased-corrected Hedges’s d as a measure of effect
size (d1), that is, the magnitude of the overall treatment
effect (Hedges and Olkin 1985). The difference between
responses of experimental and control groups was divided
by their pooled standard deviation and corrected to remove bias as a result of small sample sizes (Hedges and
Olkin 1985; Gurevitch et al. 1992). As a convention, the
magnitude of the effect size is viewed as being small if
control and treatment groups were 0.2 standard deviations
apart (d p 0.2), medium if d p 0.5, large if d p 0.8, and
very large if d 1 1.0 (Cohen 1969). The effect was judged
statistically significant if the confidence intervals of the
effect size excluded 0. Predator removal was expected to
have a positive effect on the abundance of herbivores. The
same suppression effect, however, would be revealed by a
reduction in herbivore numbers in studies in which predators were experimentally enhanced. Thus, the effect size
in predator-enhancement experiments was multiplied by
21 in order to pool effect size from both types of predatormanipulation studies (Gurevitch et al. 1992; Rosenberg et
al. 1997). As a convention, our references to the effects of
“predator removal” throughout the manuscript thus include both predator-removal and predator-enhancement
comparisons. We used the mixed meta-analysis model to
calculate the cumulative effect size for individual grouping
categories as a result of its more realistic assumptions compared to more conventional fixed-effect models (Gurevitch
and Hedges 1993; Rosenberg et al. 1997).
We identified 57 experimental papers on terrestrial trophic
cascades. Our data set included papers published between
1960 and 1999, with the majority coming from the 1980s
and 1990s (fig. 1). Our literature search suggested that
arthropod-centered investigations are currently the only category of studies providing a sufficient database for a meaningful overview. Schmitz et al. (2000) report a similar finding and identify only one observational paper (McLaren
Figure 1: Trend in research publications on terrestrial trophic cascades
based on our literature survey.
266 The American Naturalist
and Peterson 1994) and one experimental study (Gutiérrez
et al. 1997) in which indirect effects of predation on primary
production via mammalian herbivores were addressed.
Other experiments that measured effects of mammalian
grazers on vegetation did not simultaneously provide information on the indirect effects of predators on trophic
dynamics in these systems (e.g., Tansley and Adamson 1925;
Collins et al. 1998). Thus, our review focuses exclusively on
studies of arthropod-dominated webs. Studies with vertebrates were included if these groups were experimentally
manipulated as predators of arthropods in the food web
(e.g., birds, lizards). Our trophic groups correspond to
Schoener’s (1989) categories of trophic elements, including
small phytophagous herbivores (folivorous arthropods),
small carnivores (predaceous arthropods), and medium carnivores (vertebrate predators feeding on arthropods). A
conceptual justification for our focus on arthropods also
stems from the fact that these taxa constitute the most abundant and diverse group of terrestrial animals (Southwood
1978; Erwin 1982; Wilson 1987; Samways 1994) and are
significant components of most terrestrial food webs (Polis
1991; Schoenly et al. 1991).
Forty studies satisfied our selection criteria and made
up the final database, yielding 299 individual comparisons
(“experiments”) evaluating effects of predator manipulation on herbivore density, plant damage, and plant biomass
(table 1). In the majority of experiments (83%), predator
densities were lower in the experimental treatment than
in the control (ambient levels). Predator-enhancement
manipulations were found exclusively in crop systems. The
impact on the analysis of including predator-enhancement
experiments is evaluated and discussed below.
We excluded studies that used an unreplicated design,
did not report appropriate measures of variance, or employed laboratory tests. Almost 60% of the studies included effects of predator manipulation on plant damage,
and 64% used changes in plant biomass as an indicator
of trophic cascades. More than one-third of all studies did
not include any data on herbivore responses to predator
manipulations, and only five studies assessed predation
effects on all three response variables (table 1; Wright et
al. 1960; Coaker 1965; Mowat and Martin 1981; Zehnder
and Hough-Goldstein 1990; Marquis and Whelan 1994).
Publication Bias
Over 40% of the experiments measuring predator effects
on herbivore density originated from the work of three
groups of authors: Altegrim (1989; 10% of comparisons),
Schmitz (1993, 1994, 1998; Schmitz et al. 1997; 12%) and
papers and unpublished data sets of Snyder, Tuntibunpakul, and Wise (21%). Papers of Spiller and Schoener
(1990, 1994) provided the single largest set of comparisons
on plant damage (20%), and almost half of the comparisons on plant biomass effects came from the work of
Wise and his colleagues (22%) and Schmitz and his colleagues (25%). However, we found no evidence that the
mean effect sizes (d1) of these individual groups and the
rest of the data set in each response category were statistically different (herbivore density—Altegrim vs.
others: [d 5 95% CI]1.10 5 0.55 vs. 0.73 5 0.18, Qb p
1.59, df p 1, P p .21; Wise et al. vs. others: 0.66 5
0.42 vs. 0.79 5 0.18, Qb p 0.31, df p 1, P p .58; Schmitz
et al. vs. others: 0.53 5 0.44 vs. 0.80 5 0.18, Qb p 1.27,
df p 1, P p .26; plant biomass—Wise et al. vs. others:
20.15 5 0.41 vs. 20.33 5 0.19, Qb p 0.64, df p 1,
P p .42; Schmitz et al. vs. others: 20.10 5 0.30 vs.
20.39 5 0.20, Qb p 2.49, df p 1, P p .11). The exception was Spiller and Schoener versus others in the plant
damage category, where the difference was marginally significant (0.29 5 0.67 vs. 1.02 5 0.31, Qb p 3.77, df p
1, P p .052). Thus, the extent of any bias in our selection
of data set as a result of including groups of nonindependent comparisons originating from a unique research
group likely was minimal.
Plotting the effect size against sample size in all experiments (n p 299) produced a predicted funnel-shaped
pattern showing a greater variation in effect size in experiments with smaller sample sizes because of an increased sampling error (Light and Pillemer 1984; Palmer
1999). The absence of selective reporting is often indicated
by a symmetrical shape of the scatter funnel (Light and
Pillemer 1984; Palmer 1999). The shape of the scatter funnel was reasonably symmetric in our study (fig. 2), and
thus, we were confident that the bias in estimating average
effect size as a result of selective reporting was low.
Overall Magnitude of Terrestrial Trophic Cascades
Predator-Prey Link. Predators must exert sufficient pressure initially to trigger a chain of trophic interactions (i.e.,
to become “functionally significant”; Fretwell 1977; Polis
1994). Prey defense mechanisms (Owen 1980; Witz 1990),
effects of habitat refugia (Pimentel 1961), and dilution of
predation pressure because of widespread omnivory (Polis
et al. 1989; Polis 1991) may limit predator effectiveness,
reducing top-down forces to an “incidental” mortality factor (Errington 1956). When all studies were considered
together, lowering predation pressure had a large positive
effect on the abundance of terrestrial plant-feeding arthropods ([d1 5 95% CI] 0.77 5 0.16; fig. 3). Overall,
our findings support the generalization that predation can
exert a significant pressure on herbivore populations in a
wide range of terrestrial communities (Sih et al. 1985;
Henttonen et al. 1987; Floyd 1996; Polis 1999).
Table 1: Source data for the analysis of terrestrial trophic cascades
No. of comparisons per
reference measuring effects
of predator manipulation
Reference
Predatorsa
Herbivores
Plants
Producer Herbivore Plant
Plant
category
density damage biomass
Data source
Altegrim 1989
Beckerman et al. 1997
Bock et al. 1992
Brust 1994
Brust et al. 1985
Carter and Rypstra 1995
Chase 1996
Clark et al. 1994
Coaker 1965
Dial 1992
Birds
Spiders
Birds
GAPC
GAPC
Spiders
Spiders
GAPC
GAPC
Spiders, lizards
Complex
Grasshoppers
Grasshoppers
CPB
LL
Complex
Grasshoppers
LL
DL
Complex
Bilberry shrubs
Grasses, forbs
Grasses, forbs
Potato
Corn
Soybeans
Grasses, forbs
Corn
Cauliflower, cabbage
Tabonuco trees
Woodland
Grassland
Grassland
Crop
Crop
Crop
Grassland
Crop
Crop
Woodland
14
2
9
…
…
…
…
…
8
4
5
4
…
2
6
5
…
1
2
1
…
…
6
2
…
…
4
…
10
…
Dyer and Letourneau 1999
Fowler et al. 1991
Gómez and Zamora 1994
Gould and Jeanne 1984
Helenius 1990
Letourneau and Dyer 1998
Mansour and Whitcomb 1986
Mansour et al. 1985
Marquis and Whelan 1994
Moran and Hurd 1998
Moran et al. 1996
Mowat and Martin 1981
Pacala and Roughgarden 1984
Polis and Hurd 1996
Riechert and Bishop 1990
Ants, clerid beetles
Birds
Parasitoid wasps
Polistes wasps
GAPC
Ants, clerid beetles
Spiders
Spiders
Birds
Mantids
Mantids
GAPC
Spiders, lizards
Spiders
GAPC
Complex
Grasshoppers
Weevils
LL
Aphids
Complex
Scale insects
LL
Complex
Complex
Complex
DL
Complex
Complex
Complex
Woodland
Grassland
Woodland
Crop
Crop
Woodland
Crop
Crop
Woodland
Grassland
Grassland
Crop
Woodland
Woodland
Crop
…
10
1
…
4
…
1
1
2
4
3
1
1
…
11
1
…
…
…
…
4
1
1
2
…
…
1
1
1
7
1
1
1
2
5
4
…
…
2
4
1
1
…
…
…
Risch and Carroll 1982
Schmitz 1993
Schmitz 1994
Schmitz 1998
Schmitz et al. 1997
Snyder and Wise 1999
Ants
Spiders
Spiders
Spiders
Spiders
Carabids, spiders
LL
Grasshoppers
Grasshoppers
Grasshoppers
Grasshoppers
Complex
Crop
Grassland
Grassland
Grassland
Grassland
Crop
2
2
2
10
2
6
1
…
…
…
…
…
…
2
4
14
4
10
Table 1
Figure 6
Table 3; figure 3
Table 3; figures 4, 5
Figures 5, 6
Tables 1, 2; figure 4
Snyder and Wise, in press
Carabids, spiders
Complex
Ant plants
Grasses, forbs
Crucifer shrubs
Cabbage
Oats
Ant plants
Citrus trees
Avocado trees
White oak
Grasses, forbs
Grasses, forbs
Cauliflower
Complex
Atriplex shrubs
Broccoli, Brussels sprouts,
cabbage, potato, radish,
tomato
Squash
Grasses, forbs
Grasses, forbs
Grasses, forbs
Grasses, forbs
Beans, cabbage, cucumber,
eggplant, squash
Cucumber, squash
Figures 1, 2
Table 1; figure 2
Table 1; figure 6
Text; table 2
Figure 1
Figure 3
Figure 3
Figure 1b
Tables 2, 3, 8
Figures 3.11, 3.15,
3.19, 3.21
Figure 3
Text; table 3
Text
Table 3
Figures 2, 3
Figure 5
Table 2
Table II
Figure 2
Figures 4a, 6
Figures 4b, 5
Table II
Text; figure 1
Table 26.5
Table 4; figures 2, 3
6
…
6
Crop
Figures 5, 6, 7
Table 1 (Continued )
No. of comparisons per
reference measuring effects
of predator manipulation
Reference
Predatorsa
Herbivores
Plants
Producer Herbivore Plant
Plant
category
density damage biomass
Spiller and Schoener 1990
Spiller and Schoener 1994
Stoner 1993
Tuntibunpakul 1999
Spiders, lizards
Spiders, lizards
GAPC
GAPC
Complex
Complex
CPB
Complex
Sea grapes
Sea grapes
Potato
Cucumber, potato,
soybeans
Woodland
Woodland
Crop
Crop
…
6
…
16
8
6
1
3
…
…
1
5
Warrington and Whittaker 1985
Whittaker and Warrington 1985
Wright et al. 1960
Zehnder and Hough-Goldstein 1990
Ants
Ants
GAPC
GAPC
Complex
Complex
DL
CPB
Sycamore trees
Sycamore trees
Cauliflower
Potato
Woodland
Woodland
Crop
Crop
…
…
2
3
3
…
3
1
…
1
3
1
Data source
Figure 2
Figures 6, 8
Table 1; figure 6
Figures 6, 7, 21,
23, 24, 27, 29,
30, 39, 40, 41,
42
Table 4
Table 8
Tables 1, 2, 3
Tables 2, 4, 7, 8
Note: GAPC p Ground arthropod predator complex (includes studies where a diverse assemblage of predators was manipulated simultaneously; e.g., spiders, harvestmen, predaceous beetles, ants);
CPB p Colorado potato beetles; LL p Lepidoptera larvae; DL p Diptera larvae.
a
Manipulated trophic level. This category includes groups that we considered to be most likely impacted by manipulations. Our designations did not always correspond to the one suggested by
the author.
Terrestrial Trophic Cascades 269
Figure 2: Relationship between the magnitude of effect size (Hedges d1)
and the experimental sample size. Each point represents a unique
comparison.
Herbivore-Plant Link. To maintain cascading effects
throughout the community, predators must be trophically coupled with potentially strong groups of herbivores, that is, guilds capable of inflicting strong grazing
pressure on primary producers (Polis 1994, 1999). Effective plant defense mechanisms (Murdoch 1966; Feeny
1970; Coley et al. 1985) and low nutritional quality of
food (Sinclair 1975; White 1978; Batzli 1986) in some
systems, as well as the influence of the abiotic environment (Davidson and Andrewartha 1948; Ehrlich and
Birch 1967), may reduce herbivore effectiveness, rendering them a donor-controlled entity (Polis 1999; but see
Chase 1996). Changes in herbivore populations, nevertheless, cascaded through the trophic chain, increasing
the incidence of plant injury (d1 p 0.88 5 0.25; fig. 3).
Although increased populations of herbivores increased
plant damage, the overall reduction in primary production (plant biomass) was small to medium but statistically
significant (d1 p 20.32 5 0.19; fig. 3). Significant cascading trends were also found when data were analyzed
using log response ratios. On average, lowering predation
pressure increased herbivore abundance; that is, X e (experimental treatment mean) p 150.4% of the control treatment, X c (95% CI p 139.1%–162.6%), and increased plant
damage, X e p 169.4% of X c (151.5%–189.4%). Effects of
predation on plant biomass, however, were weaker; X e p
0.89% of control (0.82%–0.97%).
Cascading trophic effects are expected to be buffered at
each trophic-level transition as a result of system complexity
and time lags in responses of individual consumer groups
(Carpenter et al. 1985; Strong 1992; Polis 1994). Our data
are not consistent with this prediction, since the responses
of herbivores and primary producers measured at the level
of plant damage were similar in magnitude (fig. 3). How-
ever, the degree to which trophic cascades were dampened
at the level of primary producers could have been confounded in our analysis by the absence of data on herbivore
abundance in 31% of studies. Thus, we further analyzed a
subset of comparisons where effects of predation on herbivory and at least one of the plant performance parameters
were measured simultaneously. We found significant positive relationships between the magnitude of response of
herbivores and the amount of plant damage with either
estimator of effect size (fig. 4), which further supports the
hypothesis of trophic cascades. A slope of 1.20 for the regression, however, suggests a slight heightening of the cascade at the level of plant damage. Removal of three outliers
from the data set (a four-level cascade with lizards and
spiders: Pacala and Roughgarden 1984; small-sized branch
enclosures: Mansour and Whitcomb 1986; Mansour et al.
1985) preserved the statistical significance of this relationship in figure 4A but lowered the model’s predictive power
(n p 31, R 2 p 0.31, F p 13.18, P ! .01) and suggested a
dampening effect (slope p 0.85). Analysis with ln (RR)
showed a similar dampening of the trophic cascade
(slope p 0.89; fig. 4B).
Absence of a stronger dampening of the trophic cascade
at the level of plant herbivory may have at least two explanations. For example, behaviorally mediated cascades,
where the presence of predators may inhibit feeding of
herbivores, can significantly alter levels of herbivory without changes in herbivore densities (Schmitz 1994; Beckerman et al. 1997; Moran and Hurd 1998; Snyder and
Wise 2000). Alternatively, densities of irrelevant herbivore
species may have been assessed in experiments. Since the
overwhelming majority of predators in the surveyed experiments were generalist predators, it is possible that their
Figure 3: Overall mean effect size (595% CI) of lowering predation
pressure on the abundance of herbivores, extent of plant damage, and
changes in plant biomass across all experiments. Numbers above or below
bar graphs indicate the number of comparisons within each category.
270 The American Naturalist
level needed to impede its production significantly, a result
of diffused herbivory in the system. Thus, this “heterogeneity” (Hunter and Price 1992) or “differentiation” (Strong
1992) in consumer feeding may have modified the strength
of the trophic cascade at both the predator-herbivore as well
as the herbivore-plant trophic link.
Variations in the Magnitude and Length of Chains
of Trophic Cascades
Figure 4: Association between the magnitude of response of herbivores
and primary producers to experimental lowering of predation pressure,
estimated with (A) Hedges d1 (plant damage: n p 34, R2 p 0.68, F p
69.33, P ! .001; plant biomass: n p 68, R2 p 0.01, F p 0.65, P p .423)
and (B) log response ratios (plant damage: n p 33, R2 p 0.33, F p
15.34, P ! .001; plant biomass: n p 68, R2 p 0.05, F p 3.76, P p .06).
M1 p Mansour et al. 1985; M2 p Mansour and Whitcomb 1986; P p
Pacala and Roughgarden 1984.
effects on plant damage may have been partially channeled
via groups of herbivores that were not the focus of an
investigation.
The relationship between the change in herbivore density and change in plant biomass was weaker and only
marginally significant when analyzed with log response
ratios (fig. 4B). A strong dampening effect was suggested
at this level (d1 slope p 20.07, ln (RR) slope p 20.34).
The use of log ratios slightly improved the fit of the model
because of a logarithmic transformation of the relationship. Thus, although clear trophic cascades were detectable
for plant damage from herbivory, further effects were
strongly buffered, producing either no or only minimal
reductions in the overall plant community biomass.
These results are similar to those of Schmitz et al. (2000),
who found much stronger effects of predation on plant
damage than plant biomass. This suggests that plants had
the ability to tolerate significant levels of herbivory without
suffering highly adverse effects on primary production.
Likewise, it is plausible that, if the plant community is sufficiently diverse, the amount of herbivory inflicted on a
particular plant species may not reach the critical threshold
A more detailed inspection of the data revealed several
intriguing results. A total of 77% of the experiments
showed positive responses of herbivores to predator removal (fig. 5A). The overall magnitude of this positive
response was very large and highly significant (d1 p
1.10 5 0.18). In contrast, herbivore populations declined
following predator removal in only about 20% of cases,
and the absolute magnitude of this negative effect was
almost 3.5 times lower (d1 p 20.32 5 0.19). Plant damage mirrored the extent of herbivore responses to predator
removal. Predator removal increased plant damage in 76%
of cases, and this effect was very large (d1 p 1.38 5
0.27). Negative effects of predator removal on plant damage were again less frequent (20%) and weaker (d1 p
21.03 5 0.31; fig. 5B). Removing predators most frequently reduced plant biomass (63%), and overall this
effect was large (d1 p 20.73 5 0.15). Reverse trophic responses were weaker (d1 p 0.37 5 0.16) and less common (34%; fig. 5C). Analysis with ln (RR) produced very
similar results (fig. 5D–5F ).
According to theory, removal of top predators in food
webs with an odd number of trophic levels should boost
herbivory and reduce plant biomass (Hairston et al. 1960;
Fretwell 1977; Oksanen et al. 1981). A reverse scenario
should be prevalent in systems characterized by four (an
even number) of trophic levels. Our analysis suggests that
the overwhelming majority of terrestrial systems we reviewed behaved as odd-trophic-level systems. Increases in
the number of trophic links (i.e., interactions across more
than three trophic levels) appeared to reduce the frequency
of trophic cascades and to attenuate their magnitude.
Omnivory and Terrestrial Trophic Cascades
Widespread trophic-level omnivory is cited as one factor
causing trophic cascades to dissipate in terrestrial food
webs (Polis 1991, 1994; Polis and Strong 1996). It is interesting that all but two experiments (parasitoids: Gómez
and Zamora 1994) in our data set included generalist predators (table 1). However, solely using dietary data to predict the strength of trophic links and consequent cascading
effects may not be adequate. A maze of seemingly complex
trophic links may make it difficult to recognize community
Terrestrial Trophic Cascades 271
Figure 5: Frequency distribution of the magnitude and direction of predator-removal effects on herbivore densities, amount of plant damage, and
amount of plant biomass using Hedges d1 (A–C) and log response ratios (ln(RR); D–F ) as estimates of effect size. White and black bars denote
negative and positive values of effect size, respectively.
subsystems (modules; sensu Paine 1980; Holt 1996) that
exhibit strong internal ties. Experimental manipulations
may be a more appropriate approach to identify major
interaction pathways in communities (Paine 1980; Wise
1984, 1993; Hairston 1994). For example, although praying
mantids are generalist arthropod predators that consume
a wide range of herbivore taxa (Reitze and Nentwig 1991)
as well as other generalist predators (e.g., spiders: Moran
et al. 1996; Moran and Hurd 1998), experiments show
that mantids can evoke significant top-down effects and
boost plant biomass (Moran et al. 1996; Moran and Hurd
1998; table 2). This result reveals a mantid-herbivore-plant
module embedded in a matrix of complex feeding links
in the successional grassland community (Moran and
272 The American Naturalist
Table 2: Variation in the effect of predation by major predatory
groups on herbivore density, plant damage, and biomass
Response variable
and predator
group
Herbivore density:
GAPC
Mantids
Spiders
Birds
Lizards
Arthropods
Vertebrates
Plant damage:
GAPC
Mantids
Spiders
Birds
Lizards
Arthropods
Vertebrates
Plant biomass:
GAPC
Mantids
Spiders
Birds
Lizards
Arthropods
Vertebrates
No. of
comparisons
Effect
size
(d1)
57
7
25
35
8
90
43
95% CI
Lower
Upper
.85
.81
.61
.68
.85
.79
.71
.59
.39
.22
.42
.07
.57
.47
1.11
1.23
1.00
.93
1.61
1.01
.95
31
…
15
7
13
51
20
1.34
…
.61
1.12
.54a
.92
.81
1.00
…
.01
.54
2.10
.61
.40
1.68
…
1.21
1.69
1.17
1.22
1.22
43
5
30
9
…
86
9
2.53
2.62
2.17a
2.23a
…
2.33
2.23a
2.85
21.10
2.50
2.68
…
2.55
2.70
2.20
2.14
.17
.21
…
2.11
.23
Note: GAPC p ground arthropod predator complex.
a
Statistically not significant (95% CI includes 0).
Hurd 1998). However, Strong et al. (1999) argue that these
modules or “vignettes” are vulnerable trophic connections
that may collapse upon influence from the environment
in which they are nested. A high potential for intraguild
predation among predators or competition among herbivores and among plants may modulate the intensity of
interactions within vignettes (Strong et al. 1999).
The multichannel omnivory model (Polis 1994; Polis
and Hurd 1996; Polis and Strong 1996) further predicts
that the ability of predators to feed and to survive on
alternative food resources may modify the extent to which
generalist feeders control their resources. Thus, rather than
diluting trophic cascades, acquiring resources from a
multitude of sources may in fact facilitate their occurrence
in complex terrestrial food webs (Polis and Strong 1996;
Polis 1999). This point appears to be supported in our
review by a number of examples in which manipulated
predator species may derive substantial nutritional provisions from alternative detrital channels. Both anoles
(Dial 1992; Spiller and Schoener 1996) and spiders (Pacala
and Roughgarden 1984; Polis and Hurd 1996; Spiller and
Schoener 1996) feed on detritovorous Diptera, and ar-
thropod predators in the crop system of Wise and his
colleagues (Snyder and Wise 1999, in press; Tuntibunpakul
1999) may be subsidized by feeding on Collembola (D.
M. McNabb, J. Halaj, and D. H. Wise, unpublished data).
Thus, both facets of omnivory, that is, the provision of
energy subsidies coupled with a diffusion of feeding links,
have the potential to cast the traditional linear model of
the trophic cascade (Hairston et al. 1960) into a more
reticulate version, in which the strength of top-down control may vary widely among consumers and is more difficult to predict.
Clearly, our findings indicate that generalist predators
have the ability to trigger significant cascading effects. These
results, however, do not directly address the more challenging question of whether, and to what extent, this capacity to generate cascades is buffered by their multiresource
feeding? Comparing the magnitude of cascading effects induced by generalist and specialist natural enemies would
address this question. Although evidence exists that specialized natural enemies (e.g., insect parasitoids) can significantly suppress herbivore populations, the extent of this
trophic effect is highly variable (Murdoch et al. 1985; Hawkins 1992; Hawkins and Gross 1992; Faeth 1994; Hawkins
et al. 1999), and its consequences for plant fitness are largely
unknown (Faeth 1994). Hawkins (1992) even points out
that top-down control in many parasitoid-based food webs
may be minimal or absent. Our review of cascades generated
by generalist predators reveals that effects on herbivore densities and the level of herbivory are not necessarily reliable
predictors of their impact on plant production. Thus,
whether or not natural enemy specialists can trigger stronger
cascading effects than generalists is open to speculation at
the moment as a result of a lack of sufficient experimental
evidence.
Effects of Primary Producer Quality on
Terrestrial Trophic Cascades
We further divided studies into broad categories defined
in terms of primary producers, rates of primary production, and habitat complexity. Crop systems were predominantly annual monocultures, with the exception of two
studies that studied trophic cascades in perennial plantations (citrus: Mansour and Whitcomb 1986; avocado:
Mansour et al. 1985). The grassland category included
perennial grasses and forb vegetation of natural prairies
and successional old-field systems. Shrubby and woody
vegetation of scrublands and temperate and tropical forests
were jointly characterized as woodlands. This categorization allowed us to make comparisons along a gradient of
ecosystem productivity/habitat complexity, that is, crops
versus grasslands versus woodlands, and to contrast managed (crops) versus natural (grasslands 1 woodlands) sys-
Terrestrial Trophic Cascades 273
tems. Although this classification is very broad, a more
detailed community resolution is not feasible with the
available data set.
The quality of primary producers plays a significant role
in consumer interactions (Feeny 1970; Sinclair 1975; Fretwell 1977; White 1978; Oksanen et al. 1981). Our results
showed that the magnitude of trophic cascades varied significantly among community types. Although effects of predation on herbivores were similar in all three categories,
differences were found in effects on primary producers (table 3). Net effects of trophic cascades on plants were very
strong in crop communities, showing characteristics of oddtrophic-level systems; in the majority of experiments, predator removal increased herbivory (d1 p 1.14 5 0.25) and
reduced primary production (d1 p 20.98 5 0.34; fig. 6A).
The reverse scenario was less frequent and statistically not
significant (fig. 6A). This finding may not be surprising
considering the vulnerability and homogeneity of crop
systems.
Effects of trophic cascades were less predictable in more
complex grassland communities. Despite strong predation
effects on herbivores, there was no overall effect on plant
damage, and the effect on plant biomass was almost 60%
lower compared to crops (table 3; fig. 6). It appears that
the higher variability in plant nutritional quality, lower overall plant quality, and higher habitat diversity of grasslands
compared to crop systems may dampen overall effects of
changing herbivore densities on plant biomass in grasslands.
Moran and Hurd (1998) report detectable effects of a
trophic cascade triggered by mantid predation on grasses
but not on forbs, which contain higher levels of secondary
compounds. Reduction in the biomass of more palatable
plant resources may often be offset by an increase in the
biomass of less preferred species, thus reversing and blurring
Table 3: Magnitude of terrestrial trophic cascades in different
community types
Response variable
and plant
community type
Herbivore abundance:
Crops
Grasslands
Woodlands
Plant damage:
Crops
Grasslands
Woodlands
Plant biomass:
Crops
Grasslands
Woodlands
a
No. of
comparisons
Effect
size
(d1)
Lower
Upper
61
44
28
.92
.51
.93
.66
.26
.56
1.19
.76
1.30
35
4
32
1.60
.15a
.35
1.22
21.16
.02
1.99
1.45
.67
46
40
9
2.48
2.20
2.01a
2.77
2.38
2.72
2.19
2.03
.71
Statistically not significant (95% CI includes 0).
95% CI
Figure 6: Overall mean effect sizes (595% CI) and frequency of threeand four-level trophic cascades in crops (A), grasslands (B), and woodlands (C). Numbers above bar graphs indicate the number of comparisons within each category. ns p statistically not significant (95% CI
includes 0).
the trophic-cascade effect (Schmitz 1994). Predator-mediated effects on herbivore foraging behavior in more complex
habitats may produce similar results (Beckerman et al.
1997). For example, in the presence of spiders, grasshoppers
switch from feeding on grasses to consumption of herb
vegetation, which provides more protection from predators.
As a result, predators generated two strong but opposing
species-level cascades (sensu Polis 1999) on herbs (d1 p
20.99 5 0.66) and grasses (d1 p 1.30 5 0.89; fig. 6B), resulting in no net effect on plant damage (d1 p 0.15 5
1.30; table 3). It is also possible that the magnitude of trophic
cascades in grasslands might have been overestimated be-
274 The American Naturalist
Figure 7: Overall magnitude of trophic cascades in crop and noncrop
communities. Numbers above bar graphs indicate the number of comparisons within each category; ns p statistically not significant (95% CI
includes 0).
cause most experiments in this system employed completely
enclosed cages. For example, effects of spider predation on
grasshoppers and plant damage and biomass (Schmitz 1993,
1994, 1998; Chase 1996; Beckerman et al. 1997; Schmitz et
al. 1997) could have been magnified by the exclusion of
alternative prey and natural enemies of spiders from experimental microcosms, or could have been related to artificially inflated rates of predator-prey encounters within
confined habitats.
Examples of significant initiation of trophic cascades
were found even in diverse woodland communities. Overall effects, however, were low for plant damage and statistically insignificant for plant biomass (table 3; fig. 6C ).
It is interesting that this pattern was produced by a mixture
of strong odd- and even-trophic-level effects on herbivory
and plant biomass consumption. For example, feeding by
lizards on homopterans indirectly benefits sea grape plants
by lowering the extent of tissue damage. At the same time,
however, predation by these vertebrates on spiders that
feed on gall midges increases gall damage to the same
producer (Spiller and Schoener 1990, 1994). Thus, the
overall indirect impact of lizard predation on plants was
not significant (table 2). Strong three-trophic-level effects
of bird and ant predators in temperate forests (Warrington
and Whittaker 1985; Whittaker and Warrington 1985; Altegrim 1989; Marquis and Whelan 1994) contrast with
four-level trophic cascades on Piper trees triggered by predaceous Tarsobaenus beetles in a tropical rain forest (Letourneau and Dyer 1998; Dyer and Letourneau 1999). Although in some systems indirect effects of predation on
plant damage were observed over wider areas (e.g., Spiller
and Schoener 1997; Dyer and Letourneau 1999), trophic
cascades in these systems occurred only on single plant
species in otherwise diverse systems, and consequences of
herbivory to plant biomass production and fitness were
unclear. Thus, community-wide effects of trophic cascades
were low in woodlands.
Contrasting crop with noncrop communities yielded an
intriguing pattern. Although effects on herbivore abundance
were similar in both types of systems, the amount of herbivory following the relaxation of predation rates was significantly higher in crop than noncrop systems as suggested
by their nonoverlapping 95% confidence intervals (crop:
d1 p 1.60 5 0.36, 95% CI; noncrop: d1 p 0.32 5 0.29;
fig. 7). Crop systems also suffered significant reductions in
plant biomass (d1 p 20.48 5 0.31), whereas net effects of
trophic cascades at the level of primary production were
not statistically detectable in noncrop communities
(d1 p 20.20 5 0.23). Strong trophic-cascade effects in
crop communities are partly because of predator-enhancement manipulations, which were not done in other types
of communities. Although boosting predator numbers
above their natural levels increased the magnitude of plant
responses to trophic cascades (fig. 8), strong effects of predation on plant damage (d1 p 1.24 5 0.47) and biomass
(d1 p 20.40 5 0.33) were found in crops even after excluding predator-enhancement comparisons from the
analysis.
The net result of cascading effects seems to be significantly stronger in crops than natural communities. Crop
plants were the only primary producers where predator
removals occasionally resulted in “runaway consumption”
Figure 8: Overall magnitude of trophic cascades in predator-removal
and predator-enhancement comparisons. Numbers above bar graphs indicate the number of comparisons within each category. Note that the
absolute magnitude of effect size is compared here; the sign for predator
enhancement experiments was reversed during analyses to enable pooling
of effects (Rosenberg et al. 1997).
Terrestrial Trophic Cascades 275
(sensu Strong 1992) of plants, producing “cleared substrate” effects (e.g., Wright et al. 1960, figs. 1–3; Snyder
and Wise, in press). Trophic cascades in crops thus may
represent a very special form of community-level cascade
in which a few (vulnerable) plant species dominate the
system (Polis 1999). This result presents a fascinating analogy with cascading effects causing “clear water” phenomena in aquatic systems (Carpenter et al. 1985; Power 1990;
Strong 1992).
Polis (1994) argues that trophic cascades are more likely
to occur in a low-disturbance environment, with low spatial
and temporal heterogeneity. The stochastic disruption hypothesis (Schoener 1993) further predicts that chance events
such as weather variability may disrupt indirect effects by
eliminating critical species or trophic links from a food web.
The occurrence of strong cascades in crop communities,
which experience significant periodical disturbances, does
not support the prediction that high-disturbance environments weaken trophic cascades. Hawkins et al. (1999) argue
that top-down control is more frequently observed in managed than natural systems as a result of the simpler habitat
and food web structure of managed systems. Thus, it appears that release of herbivores from predation pressure
nested within a structurally and species-simple environment
with highly susceptible plant resources may explain the
greater propensity of crop systems to cascade. Even though
Schmitz et al. (2000) do not include crop systems in their
review, some of their findings support our conclusions. For
example, removal of predators produced significantly
stronger effects on primary producers in low- compared to
high-diversity systems, and plant chemical defense mechanisms appeared to buffer top-down effects (Schmitz et al.
2000).
We compared our results with those of Brett and Goldman (1996; table 1) to assess the evidence that the magnitude of trophic cascades differs between terrestrial and
aquatic communities. The absolute magnitude of the
trophic cascade at the level of zooplankton (“herbivores”)
was d p 1.39 (95% CI; 0.72–2.06). Although the topdown pressure on herbivores in terrestrial food webs was
lower (d p 0.77, 0.61–0.93), this difference was not statistically significant because of overlapping confidence intervals. Even the difference between aquatic systems and
structurally simple crop habitats was statistically nonsignificant (d p 0.92, 0.66–1.19). On the other hand, the
absolute response of aquatic primary producers (phytoplankton; d p 2.01, 1.30–2.72) was significantly stronger
than that in terrestrial communities (terrestrial overall effect: d p 0.32, 0.13–0.51; crops: d p 0.48, 0.17–0.79).
This quantitative comparison strongly suggests that the
effect of trophic cascades on primary producers is significantly greater in aquatic than terrestrial systems.
Conclusions
Our results present clear experimental evidence for trophic
cascades in terrestrial communities. Since in the overwhelming majority of studies these effects were induced
by generalist predators, it appears that intraguild predation
and trophic-level omnivory alone do not preclude the possibility of strong cascading indirect effects among terrestrial consumers. However, the paucity of experimental evidence on trophic cascades induced by specialized natural
enemies prevents an assessment of the extent to which
trophic cascades are buffered by the breadth of predator
diet. Our review does provide evidence that trophic-level
omnivory contributes to the dampening of trophic cascades induced by complexes of generalist predators, because in several studies community-wide consequences for
primary production were reduced by counteractive effects
of three- and four-level cascades. Net cancellation of effects
generated by different trophic modules appeared to be less
prevalent in agricultural systems, although even in crops
such counteractive interactions can be strong (Snyder and
Wise, in press).
Although predation had large effects on herbivore densities in all systems, overall effects on plant damage and
plant biomass were highly variable in natural systems. In
addition, adverse effects of herbivory on primary production were strongly buffered at the plant level, with the
exception of crop systems where predators occasionally
produced substantial indirect effects on plant biomass. We
suggest that such effects occur, despite a strong annual
disturbance regime, as a result of a relatively simple habitat
structure and the presence of a more homogeneous and
vulnerable plant community in agricultural systems.
Despite a relatively narrow overlap in databases (21%;
17/[40 1 41] papers), our meta-analysis and that of Schmitz
et al. (2000) both found statistically significant evidence for
trophic cascades in terrestrial systems. Both meta-analyses
also revealed that trophic cascades are stronger at the level
of plant damage than plant biomass. This agreement between two independent meta-analyses strengthens the generality of the conclusions regarding the prevalence and intensity of terrestrial trophic cascades. Our joint results
should be interpreted with some caution, however. The
availability of adequate experimental evidence only from
arthropod-centered food webs biased our reviews and limits
the scope of inferences. Our understanding of terrestrial
systems in general would be much improved by including
studies with vertebrate herbivores. Such an analysis currently is not feasible and we hereby encourage these types
of studies.
We disagree with the conclusion of Schmitz et al. (2000)
that the strength and pattern of terrestrial trophic cascades
are equivalent to those of aquatic communities. Our meta-
276 The American Naturalist
analysis of the literature supports the view that terrestrial
trophic cascades represent qualitatively different indirect interactions compared to their aquatic equivalents (Strong
1992; Polis 1999). With the exception of some crop systems,
terrestrial cascades appear to be species-level phenomena.
Although residual effects of predation can cascade to primary producers in both systems, net consequences for primary producers in aquatic and terrestrial systems are different. Whereas grazing of planktonic herbivores under
no-predator regimes can substantially reduce the biomass
of the algal phytoplankton and occasionally produce community-wide effects on primary producers, this type of runaway consumption seems to be strongly buffered by terrestrial producers, suggesting a predominately bottom-up
template of community structure as suggested by White
(1978) and reiterated repeatedly by others (e.g., Hunter and
Price 1992; Strong 1992).
Do indirect effects of predation in terrestrial communities flow torrentially down the trophic waterfall, or do
they trickle? Our analysis provides a preliminary answer
for food webs dominated by generalist arthropod predators. The terrestrial cascade starts strongly but becomes
diverted to a trickle when it reaches the pool of primary
production, with the exception of those crop systems in
which the cascade continues on to cause not a ripple but
a splash.
Acknowledgments
We thank K. L. Lawrence, D. M. MacNabb, J. Moya-Laraño,
C. M. Rauter, and J. L. Williams for reading and commenting on the manuscript. J. Helenius and S. E. Riechert
generously provided their unpublished data. We also appreciate thorough and stimulating reviews by J. Gurevitch,
P. J. Morin, and D. R. Strong. This material is based upon
work supported by a National Science Foundation Postdoctoral Fellowship in Biosciences Related to the Environment (DBI-9804167) awarded to J.H. Unpublished data on
vegetable crops are from experiments supported, in part,
by U.S. Environmental Protection Agency grant G71A0056
to D.H.W. This is publication 00-08-25 of the Kentucky
Agricultural Experiment Station.
Literature Cited
Abrams, P. 1987. Indirect interactions between species that
share a predator: varieties of indirect effects. Pages
38–54 in W. C. Kerfoot and A. Sih, eds. Predation: direct
and indirect impacts on aquatic communities. University Press of New England, Hanover.
Abrams, P. A. 1993. Effect of increased productivity on the
abundances of trophic levels. American Naturalist 141:
351–371.
———. 1995. Implications of dynamically variable traits
for identifying, classifying, and measuring direct and
indirect effects in ecological communities. American
Naturalist 146:112–134.
Abrams, P. A., B. A. Menge, G. G. Mittelbach, D. A. Spiller,
and P. Yodzis. 1996. The role of indirect effects in food
webs. Pages 371–395 in G. A. Polis and K. O. Winemiller, eds. Food webs: integration of patterns and dynamics. Chapman & Hall, New York.
Altegrim, O. 1989. Exclusion of birds from bilberry stands:
impact on insect larval density and damage to the bilberry. Oecologia (Berlin) 79:136–139.
Beckerman, A. P., M. Uriarte, and O. J. Schmitz. 1997.
Experimental evidence for a behavior-mediated cascade
in a terrestrial food chain. Proceedings of the National
Academy of Sciences of the USA 94:10735–10738.
Begon, M., J. L. Harper, and C. R. Townsend. 1996. Ecology: individuals, populations and communities. Blackwell Science, London.
Batzli, G. O. 1986. Nutritional ecology of the California
vole: effects of food quality on reproduction. Ecology
67:406–412.
Billick, I., and T. J. Case. 1994. Higher order interactions
in ecological communities: what are they and how can
they be detected? Ecology 75:1529–1543.
Bock, C. E., J. H. Bock, and M. C. Grant. 1992. Effects of
bird predation on grasshopper densities in an Arizona
grassland. Ecology 73:1706–1717.
Brett, M. T., and C. R. Goldman. 1996. A meta-analysis of
the freshwater trophic cascade. Proceedings of the National Academy of Sciences of the USA 93:7723–7726.
———. 1997. Consumer versus resource control in freshwater pelagic food webs. Science (Washington, D.C.)
275:384–386.
Brooks, J. L., and S. I. Dodson. 1965. Predation, body size,
and composition of plankton. Science (Washington,
D.C.) 150:28–35.
Brust, G. E. 1994. Natural enemies in straw-mulch reduce
Colorado potato beetle populations and damage to potato. Biological Control 4:163–169.
Brust, G. E., B. R. Stinner, and D. A. McCartney. 1985.
Tillage and soil insecticide effects on predator–black
cutworm (Lepidoptera: Noctuidae) interactions in corn
agroecosystems. Journal of Economic Entomology 78:
1389–1392.
Carpenter, S. R., J. F. Kitchell, and J. R. Hodgson. 1985.
Cascading trophic interactions and lake productivity.
BioScience 35:634–639.
Carpenter, S. R., J. F. Kitchell, J. R. Hodgson, P. A. Cochran,
J. J. Elser, M. M. Elser, D. M. Lodge, D. Kretchmer, X.
He, and C. N. von Ende. 1987. Regulation of lake primary productivity by food web structure. Ecology 68:
1863–1876.
Carter, P. E., and A. L. Rypstra. 1995. Top-down effects in
Terrestrial Trophic Cascades 277
soybean agroecosystems: spider density affects herbivore
damage. Oikos 72:433–439.
Chase, J. M. 1996. Abiotic controls of trophic cascades in
a simple grassland food chain. Oikos 77:495–506.
Clark, M. S., J. M. Luna, N. D. Stone, and R. R. Youngman.
1994. Generalist predator consumption of armyworm
(Lepidoptera: Noctuidae) and effect of predator removal
on damage in no-till corn. Environmental Entomology
23:617–622.
Coaker, T. H. 1965. Further experiments on the effect of
beetle predators on the numbers of the cabbage root
fly, Erioischia brassicae (Bouché), attacking brassica
crops. Annals of Applied Biology 56:7–20.
Cohen, J. 1969. Statistical power analysis for the behavioral
sciences. Academic Press, New York.
Coley, P. D., J. P. Bryant, and F. S. I. Chapin. 1985. Resource
availability and plant antiherbivore defense. Science
(Washington, D.C.) 230:895–899.
Collins, S. L., A. K. Knapp, J. M. Briggs, J. M. Blair, and
E. M. Steinauer. 1998. Modulation of diversity by grazing and mowing in native tallgrass prairie. Science
(Washington, D.C.) 280:745–747.
Connell, J. H. 1983. On the prevalence and relative importance of interspecific competition: evidence from
field experiments. American Naturalist 122:661–696.
Davidson, J., and H. G. Andrewartha. 1948. The influence
of rainfall, evaporation and atmospheric temperature on
fluctuations in the size of a natural population of Thrips
imaginis (Thysanoptera). Journal of Animal Ecology 17:
200–222.
Dial, R. 1992. A food web for a tropical rain forest: the
canopy view from Anolis. Ph.D. diss. Stanford University,
Stanford, Calif.
Dyer, L. A., and D. K. Letourneau. 1999. Trophic cascade
in a complex terrestrial community. Proceedings of the
National Academy of Sciences of the USA 96:5072–5076.
Ehrlich, P. R., and L. C. Birch. 1967. The “balance of
nature” and “population control.” American Naturalist
101:97–107.
Englund, G., O. Sarnelle, and S. D. Cooper. 1999. The
importance of data-selection criteria: meta-analysis of
stream predation experiments. Ecology 80:1132–1141.
Errington, P. L. 1956. Factors limiting higher vertebrate
populations. Science (Washington, D.C.) 124:304–307.
Erwin, T. L. 1982. Tropical forests: their richness in Coleoptera and other arthropod species. Coleopterists Bulletin 36:74–75.
Faeth, S. H. 1994. Induced plant responses: effects on parasitoids and other natural enemies of phytophagous insects. Pages 245–260 in B. A. Hawkins and W. Sheehan,
eds. Parasitoid community ecology. Oxford University
Press, Oxford.
Feeny, P. P. 1970. Seasonal changes in oak leaf tannins and
nutrients as a cause of spring feeding by winter month
caterpillars. Ecology 51:565–581.
Floyd, T. 1996. Top-down impacts on creosotebush herbivores in a spatially and temporally complex environment. Ecology 77:1544–1555.
Fowler, A. C., R. L. Knight, T. L. George, and L. C.
McEwen. 1991. Effects of avian predation on grasshopper populations in North Dakota grasslands. Ecology
72:1775–1781.
Fretwell, S. D. 1977. The regulation of plant communities
by the food chains exploiting them. Perspectives in Biology and Medicine 20:169–185.
Goldberg, D. E., T. Rajaniemi, J. Gurevitch, and A. StewartOaten. 1999. Empirical approaches to quantifying interaction intensity: competition and facilitation along
productivity gradients. Ecology 80:1118–1131.
Gómez, J., and R. Zamora. 1994. Top-down effects in a
tritrophic system: parasitoids enhance plant fitness. Ecology 75:1023–1030.
Gould, W. P., and R. L. Jeanne. 1984. Polistes wasps (Hymenoptera: Vespidae) as control agents for lepidopterous
cabbage pests. Environmental Entomology 13:150–156.
Gurevitch, J., and L. V. Hedges. 1993. Meta-analysis: combining the results of independent experiments. Pages
378–398 in S. M. Scheiner and J. Gurevitch, eds. Design
and analysis of ecological experiments. Chapman &
Hall, New York.
———. 1999. Statistical issues in ecological meta-analysis.
Ecology 80:1142–1149.
Gurevitch, J., L. L. Morrow, A. Wallace, and J. S. Walsh.
1992. A meta-analysis of competition in field experiments. American Naturalist 140:539–572.
Gutiérrez, J. R., P. L. Meserve, S. Herrera, L. C. Contreras,
and F. M. Jaksic. 1997. Effects of small mammals and
vertebrate predators on vegetation in the Chilean semiarid zone. Oecologia (Berlin) 109:398–406.
Hairston, N. G. 1994. Ecological experiments: purpose,
design, and execution. Cambridge University Press,
Cambridge.
Hairston, N. G., F. E. Smith, and L. B. Slobodkin. 1960.
Community structure, population control, and competition. American Naturalist 94:421–425.
Hartley, M. J., and M. L. Hunter. 1998. A meta-analysis
of forest cover, edge effects, and artificial nest predation
rates. Conservation Biology 12:465–469.
Hawkins, B. A. 1992. Parasitoid-host food webs and donor
control. Oikos 65:159–162.
Hawkins, B. A., and P. Gross. 1992. Species richness and
population limitation in insect parasitoid-host systems.
American Naturalist 139:417–423.
Hawkins, B. A., N. J. Mills, M. A. Jervis, and P. W. Price.
1999. Is the biological control of insects a natural phenomenon? Oikos 86:493–506.
278 The American Naturalist
Hedges, L. V., and I. Olkin. 1985. Statistical methods for
meta-analysis. Academic Press, Boston.
Hedges, L. V., J. Gurevitch, and P. S. Curtis. 1999. The
meta-analysis of response ratios in experimental ecology. Ecology 80:1150–1156.
Helenius, J. 1990. Effect of epigeal predators on infestation
by the aphid Rhopalosiphum padi and on grain yield of
oats in monocrops and mixed intercrops. Entomologia
Experimentalis et Applicata 54:225–236.
Henttonen, H., T. Oksanen, A. Jortikka, and V. Haukisalmi. 1987. How much do weasels shape microtine cycles in the northern Fennoscandian taiga? Oikos 50:
353–365.
Holt, R. D. 1977. Predation, apparent competition, and
the structure of prey communities. Theoretical Population Biology 12:197–229.
———. 1996. Community modules. Pages 333–350 in M.
Begon, A. Gange, and V. Brown, eds. Multitrophic interactions. Chapman & Hall, London.
Holt, R. D., and J. H. Lawton. 1993. Apparent competition
and enemy-free space in insect host-parasitoid communities. American Naturalist 142:623–645.
Hrbácek, J. M., M. Dvoráková, V. Korı́nek, and L. Procházková. 1961. Demonstration of the effect of the fish
stock on the species composition of zooplankton and
the intensity of metabolism of the whole plankton association. Verhandlungen der Internationalen Vereinigung für Limnologie 14:192–195.
Hunter, M. D., and P. W. Price. 1992. Playing chutes and
ladders: heterogeneity and the relative roles of bottomup and top-down forces in natural communities. Ecology 73:724–732.
Järvinen, A. 1991. A meta-analytic study of the effects of
female age on laying-date and clutch-size in the great
tit Parus major and the pied flycatcher Ficedula hypoleuca. Ibis 133:62–67.
Kajak, A. 1997. Effects of epigeic macroarthropods on grass
litter decomposition in mown meadow. Agriculture,
Ecosystems, and Environment 64:53–63.
Kajak, A., and H. Jakubczyk. 1977. Experimental studies
on predation in the soil-litter interface. Ecological Bulletin 25:493–496.
Koricheva, J., S. Larsson, and E. Haukioja. 1998. Insect
performance on experimentally stressed woody plants:
a meta-analysis. Annual Review of Entomology 43:
195–216.
Lawrence, K. L., and D. H. Wise. 2000. Spider predation
on forest-floor Collembola and evidence for indirect
effects on decomposition. Pedobiologia 44:33–39.
Lawton, J. H. 1999. Are there general laws in ecology?
Oikos 84:177–192.
Leibold, M. A. Resource edibility and the effects of pred-
ators and productivity of the outcome of trophic interactions. American Naturalist 134:922–949.
Letourneau, D. K., and L. A. Dyer. 1998. Experimental test
in lowland tropical forest shows top-down effects
through four trophic levels. Ecology 79:1678–1687.
Light, R. J., and D. B. Pillemer. 1984. Summing up: the
science of reviewing research. Harvard University Press,
Cambridge, Mass.
MacInnes, C. D., and R. H. Kerbes. 1987. Growth of the
snow goose, Chen caerulescens, colony at McConnell
River, Northwest Territories: 1940–1980. Canadian Field
Naturalist 101:33–39.
Mansour, F., and W. H. Whitcomb. 1986. The spiders of
a citrus grove in Israel and their role as biocontrol agents
of Ceroplastes floridensis (Homoptera: Coccidae). Entomophaga 31:269–276.
Mansour, F., M. Wysoki, and W. H. Whitcomb. 1985. Spiders inhabiting avocado orchards and their role as natural enemies of Boarmia selenaria Schiff. (Lepidoptera:
Geometridae) larvae in Israel. Acta Oecologica Oecologia Applicata 6:315–321.
Marquis, R. J., and C. J. Whelan. 1994. Insectivorous birds
increase growth of white oak through consumption of
leaf-chewing insects. Ecology 75:2007–2014.
McCann, K. S., A. Hastings, and D. R. Strong. 1998.
Trophic cascades and trophic trickles in pelagic food
webs. Proceedings of the Royal Society of London B,
Biological Sciences 265:205–209.
McLaren, B. E., and R. O. Peterson. 1994. Wolves, moose,
and tree rings on Isle Royale. Science (Washington,
D.C.) 266:1555–1558.
Menge, B. A. 1995. Indirect effects in marine rocky intertidal interaction webs: patterns and importance. Ecological Monographs 65:21–74.
Moran, M. D., and L. E. Hurd. 1998. A trophic cascade
in a diverse arthropod community caused by a generalist
arthropod predator. Oecologia (Berlin) 113:126–132.
Moran, M. D., T. P. Rooney, and L. E. Hurd. 1996. Topdown cascade from a bitrophic predator in an old-field
community. Ecology 77:2219–2227.
Mowat, D. J., and S. J. Martin. 1981. The contribution of
predatory beetles (Coleoptera: Carabidae and Staphylinidae) and seed-bed-applied insecticide to the control of
cabbage root fly, Delia brassicae (Wied.), in transplanted
cauliflowers. Horticultural Research 21:127–136.
Murdoch, W. W. 1966. “Community structure, population
control, and competition”—a critique. American Naturalist 100:219–226.
Murdoch, W. W., J. Chesson, and P. L. Chesson. 1985.
Biological control in theory and practice. American Naturalist 125:344–366.
NRC (National Research Council). 1996. Ecologically based
pest management: new solutions for a new century. Com-
Terrestrial Trophic Cascades 279
mittee on Pest and Pathogen Control through Management of Biological Control Agents and Enhanced Cycles
and Natural Process. National Academy Press, Washington, D.C.
Oksanen, L., and T. Oksanen. 2000. The logic and realism
of the hypothesis of exploitation ecosystems. American
Naturalist 155:703–723.
Oksanen, L., S. D. Fretwell, J. Arruda, and P. Niemelä.
1981. Exploitation ecosystem in gradients of primary
productivity. American Naturalist 118:240–261.
Osenberg, C. W., O. Sarnelle, and S. D. Cooper. 1997.
Effect size in ecological experiments: the application of
biological models to meta-analysis. American Naturalist
150:798–812.
Osenberg, C. W., O. Sarnelle, and D. E. Goldberg. 1999.
Meta-analysis in ecology: concepts, statistics, and applications. Ecology 80:1103–1104.
Owen, D. F. 1980. Camouflage and mimicry. Oxford University Press, Oxford.
Pacala, S., and J. Roughgarden. 1984. Control of arthropod
abundance by Anolis lizards on St. Eustatius (Neth. Antilles). Oecologia (Berlin) 64:160–162.
Paine, R. T. 1966. Food web complexity and species diversity. American Naturalist 100:65–75.
———. 1980. Food webs: linkage, interaction strength and
community infrastructure. Journal of Animal Ecology
49:667–685.
Palmer, A. R. 1999. Detecting publication bias in metaanalyses: a case study of fluctuating asymmetry and sexual
selection. American Naturalist 154:220–233.
Pimentel, D. 1961. An evaluation of insect resistance in
broccoli, Brussels sprouts, cabbage, collards and kale.
Journal of Economic Entomology 54:156–158.
Polis, G. A. 1991. Complex trophic interactions in deserts:
an empirical critique of food-web theory. American
Naturalist 138:123–155.
———. 1994. Food webs, trophic cascades and community
structure. Australian Journal of Ecology 19:121–136.
———. 1999. Why are parts of the world green? multiple
factors control productivity and the distribution of biomass. Oikos 86:3–15.
Polis, G. A., and R. D. Holt. 1992. Intraguild predation:
the dynamics of complex trophic interactions. Trends
in Ecology & Evolution 7:151–154.
Polis, G. A., and S. D. Hurd. 1996. Allochthonous input
across habitats, subsidized consumers, and apparent
trophic cascades: examples from the ocean-land interface. Pages 275–285 in G. A. Polis and K. O. Winemiller,
eds. Food webs: integration of patterns and dynamics.
Chapman & Hall, New York.
Polis, G. A., and D. R. Strong. 1996. Food web complexity
and community dynamics. American Naturalist 147:
813–846.
Polis, G. A., C. A. Myers, and R. D. Holt. 1989. The ecology
and evolution of intraguild predation: potential competitors that eat each other. Annual Review of Ecology
and Systematics 20:297–330.
Power, M. E. 1990. Effects of fish in river food webs.
Science (Washington, D.C.) 250:811–814.
Power, M. E., W. J. Matthews, and A. J. Stewart. 1985.
Grazing minnows, piscivorous bass, and stream algae:
dynamics of a strong interaction. Ecology 66:1448–1456.
Reitze, M., and W. Nentwig. 1991. Comparative investigations into the feeding ecology of six Mantodea species.
Oecologia (Berlin) 86:568–574.
Riechert, S. E., and L. Bishop. 1990. Prey control by an
assemblage of generalist predators: spiders in garden test
systems. Ecology 71:1441–1450.
Risch, S. J., and C. R. Carroll. 1982. Effect of a keystone
predaceous ant, Solenopsis geminata, on arthropods in
a tropical agroecosystem. Ecology 63:1979–1983.
Rosenberg, M. S., D. C. Adams, and J. Gurevitch. 1997.
MetaWin: statistical software for meta-analysis with resampling tests. Version 1.0. Sinauer Associates, Sunderland, Mass.
Samways, M. J. 1994. Insect conservation biology. Chapman & Hall, London.
Schmitz, O. J. 1993. Trophic exploitation in grassland food
chains: simple models and a field experiment. Oecologia
(Berlin) 93:327–335.
———. 1994. Resource edibility and trophic exploitation
in an old-field food web. Proceedings of the National
Academy of Sciences of the USA 91:5364–5367.
———. 1998. Direct and indirect effects of predation and
predation risk in old-field interaction webs. American
Naturalist 151:327–342.
Schmitz, O. J., A. P. Beckerman, and K. M. O’Brien. 1997.
Behaviorally mediated trophic cascades: effects of predation risk on food web interactions. Ecology 78:
1388–1399.
Schmitz, O. J., P. A. Hambäck, and A. P. Beckerman. 2000.
Trophic cascades in terrestrial systems: a review of the
effects of carnivore removals on plants. American Naturalist 155:141–153.
Schoener, T. W. 1989. Food webs from the small to the
large. Ecology 70:1559–1589.
———. 1993. On the relative importance of direct versus
indirect effects in ecological communities. Pages
365–411 in H. Kawanabe, J. E. Cohen, and K. Iwasaki,
eds. Mutualism and community organization: behavioral, theoretical and food web approaches. Oxford University Press, Oxford.
Schoenly, K., R. A. Beaver, and T. A. Heumier. 1991. On
the trophic relations of insects: a food-web approach.
American Naturalist 137:597–638.
Sih, A., P. Crowley, M. McPeek, J. Petranka, and K. Stroh-
280 The American Naturalist
meier. 1985. Predation, competition and prey communities: a review of field experiments. Annual Review
of Ecology and Systematics 16:269–311.
Sinclair, A. R. E. 1975. The resource limitation of trophic
levels in tropical grassland ecosystems. Journal of Animal Ecology 44:497–520.
Slobodkin, L. B., F. E. Smith, and N. G. Hairstone. 1967.
Regulation in terrestrial ecosystems, and the implied
balance of nature. American Naturalist 101:109–124.
Snyder, W. E., and D. H. Wise. 1999. Predator interference
and the establishment of generalist predator populations
for biocontrol. Biological Control 15:283–292.
———. 2000. Antipredator behavior of spotted cucumber
beetles, Diabrotica undecimpunctata howardi (Coleoptera: Chrysomelidae), in response to predators that pose
varying risks. Environmental Entomology 29:35–42.
———. In press. Contrasting trophic cascades generated
by a community of generalist predators. Ecology.
Southwood, T. R. E. 1978. The components of diversity.
Symposia of the Royal Entomological Society of London
9:19–40.
Spiller, D. A., and T. W. Schoener. 1990. A terrestrial field
experiment showing the impact of eliminating top predators on foliage damage. Nature (London) 347:469–472.
———. 1994. Effects of top and intermediate predators
in a terrestrial food web. Ecology 75:182–196.
———. 1996. Food-web dynamics on some small subtropical islands: effects of top and intermediate predators. Pages 160–169 in G. A. Polis and K. O. Winemiller,
eds. Food webs: integration of patterns and dynamics.
Chapman & Hall, New York.
———. 1997. Folivory on islands with and without insectivorous lizards: an eight-year study. Oikos 78:15–22.
Stamp, N. E., and M. D. Bowers. 1991. Indirect effect on
survivorship of caterpillars due to presence of invertebrate predators. Oecologia (Berlin) 88:325–330.
Stoner, K. A. 1993. Effects of straw and leaf mulch and
trickle irrigation on the abundance of Colorado potato
beetles (Coleoptera: Chrysomelidae) on potato in Connecticut. Journal of Entomological Science 28:393–403.
Strauss, S. Y. 1991. Indirect effects in community ecology:
their definition, study and importance. Trends in Ecology & Evolution 6:206–210.
Strong, D. R. 1992. Are trophic cascades all wet? differentiation and donor-control in speciose ecosystems.
Ecology 73:747–754.
Strong, D. R., H. K. Kaya, A. V. Whipple, A. L. Child, S.
Kraig, M. Bondonno, K. Dyer, and J. L. Maron. 1996a.
Entomopathogenic nematodes: natural enemies of rootfeeding caterpillars on bush lupine. Oecologia (Berlin)
108:167–173.
Strong, D. R., J. L. Maron, and P. G. Connors. 1996b. Topdown from underground? the underappreciated influ-
ence of subterranean food webs on above-ground ecology. Pages 170–175 in G. A. Polis and K. O. Winemiller,
eds. Food webs: integration of patterns and dynamics.
Chapman & Hall, New York.
Strong, D. R., A. V. Whipple, A. L. Child, and B. Dennis.
1999. Model selection for a subterranean trophic cascade: root-feeding caterpillars and entomopathogenic
nematodes. Ecology 80:2750–2761.
Tansley, A. G., and R. S. Adamson. 1925. Studies of the
vegetation of the English chalk. III. The chalk grasslands
of the Hampshire-Sussex border. Journal of Ecology 13:
177–223.
Tonhasca, A., and D. N. Byrne. 1994. The effects of crop
diversification on herbivorous insects: a meta-analysis
approach. Ecological Entomology 19:239–244.
Tuntibunpakul, P. 1999. The impact of spiders and ground
beetles on the abundance of insect pests and yields in
soybean and vegetable agroecosystems. Ph.D. diss. University of Kentucky, Lexington.
Vanni, M. J., and D. L. Findlay. 1990. Trophic cascades
and phytoplankton community structure. Ecology 71:
921–937.
Warrington, S., and J. B. Whittaker. 1985. An experimental
field study of different levels of insect herbivory induced
by Formica rufa predation on sycamore (Acer pseudoplatanus). I. Lepidoptera larvae. Journal of Applied
Ecology 22:775–785.
White, T. C. R. 1978. The importance of a relative shortage
of food in animal ecology. Oecologia (Berlin) 33:71–86.
Whittaker, J. B., and S. Warrington. 1985. An experimental
field study of different levels of insect predation induced
by Formica rufa predation on sycamore (Acer pseudoplatanus). III. Effects on tree growth. Journal of Applied
Ecology 22:797–811.
Wilson, E. O. 1987. The little things that run the world.
Conservation Biology 1:344–346.
Wise, D. H. 1984. The role of competition in spider communities: insights from field experiments with a model
organism. Pages 54–63 in D. R. Strong, D. Simberloff,
L. G. Abele, and A. B. Thistle, eds. Ecological communities: conceptual issues and the evidence. Princeton
University Press, Princeton, N.J.
———. 1993. Spiders in ecological webs. Cambridge University Press, Cambridge.
Witz, B. W. 1990. Antipredator mechanisms in arthropods:
a twenty year literature survey. Florida Entomologist 73:
71–99.
Wootton, J. T. 1993. Indirect effects and habitat use in an
intertidal community: interaction chains and interaction modifications. American Naturalist 141:71–89.
———. 1994. The nature and consequences of indirect
effects in ecological communities. Annual Review of
Ecology and Systematics 25:443–466.
Terrestrial Trophic Cascades 281
Wright, D. W., R. D. Hughes, and J. Worrall. 1960. The
effect of certain predators on the numbers of cabbage
root fly (Erioischia brassicae [Bouché]) and on the subsequent damage caused by the pest. Annals of Applied
Biology 48:756–763.
Zehnder, G. W., and J. Hough-Goldstein. 1990. Colorado
potato beetle (Coleoptera: Chrysomelidae) population
development and effects on yield of potatoes with and
without straw mulch. Journal of Economic Entomology
83:1982–1987.
Associate Editor: Peter J. Morin