Journal of Animal Ecology 2011, 80, 696–704
doi: 10.1111/j.1365-2656.2011.01808.x
Contrasting cascade effects of carnivores on plant
fitness: a meta-analysis
Gustavo Q. Romero1* and Julia Koricheva2
1
Departamento de Biologia Animal, Instituto de Biologia (IB), Universidade Estadual de Campinas (UNICAMP), CEP
13083-970, Cx. P 6109 Campinas-SP, Brazil; and 2School of Biological Sciences, Royal Holloway, University of London,
Egham, Surrey TW20 0EX, UK
Summary
1. Although carnivores indirectly improve plant fitness by decreasing herbivory, they may also
decrease plant reproduction by disrupting plant–pollinator mutualism. The overall magnitude of
the resulting net effect of carnivores on plant fitness and the factors responsible for the variations
in strength and direction of this effect have not been explored quantitatively to date.
2. We performed a meta-analysis of 67 studies containing 163 estimates of the effects of carnivores
on plant fitness and examined the relative importance of several potential sources of variation in
carnivore effects.
3. Carnivores significantly increased plant fitness via suppression of herbivores and decreased fitness by consuming pollinators. The overall net effect of carnivores on plant fitness was positive
(32% increase), indicating that effects via herbivores were stronger than effects via pollinators.
4. Parasitoids had stronger positive effect on plant fitness than predators. Active hunters increased
plant fitness, whereas stationary predators had no significant effect, presumably because they were
more prone to disrupt plant–pollinator mutualism. Carnivores with broader habitat domain had
negative effects on plant fitness, whereas those with narrow habitat domain had positive effects.
5. Predator effects were positive for plants which offered rewards (e.g. extrafloral nectaries) and
negative for plants which lacked any attractors.
6. This study adds new knowledge on the factors that determine the strength of terrestrial trophic
cascades and highlights the importance of considering simultaneous contrasting interactions in the
same study system.
Key-words: indirect effects, indirect plant defences, pollen limitation, predator hunting mode,
top-down, trophic cascade
Introduction
Predation is one of the most important biotic processes determining population dynamics and community structure.
Direct effects of carnivores on prey density or biomass via
consumptive or nonconsumptive pathways may be transmitted indirectly to lower trophic levels in a trophic cascade.
Existence of trophic cascades has been reported in various
types of ecosystems (e.g. Strong 1992; Polis 1999; Shurin,
Gruner & Hillebrand 2006), and the strength of cascades has
been shown to depend on variation in prey and predator
metabolism and taxonomy (Schmitz, Hambäck & Beckerman 2000; Borer et al. 2005), predator mobility and thermal
regulation (Borer et al. 2005), plant anti-herbivore defences,
prey diversity (Schmitz, Hambäck & Beckerman 2000), environment (Halaj & Wise 2001; Dyer & Coley 2002; Shurin
*Correspondence author. E-mail: [email protected]
et al. 2002) and methodological differences among studies
(Schmitz, Hambäck & Beckerman 2000; Bell, Neill & Schluter 2003). Until recently, most of the research on trophic cascades has focused on positive effects of carnivores on plants
via suppression of herbivores, consistent with the ‘green
world hypothesis’ (Hairston, Smith & Slobodkin 1960).
However, carnivore effects on plant fitness may be more
complex in terrestrial ecosystems where reproduction of
many plant species depends on insect pollinators. Negative
effects of carnivores on plant fitness may arise whether predators feed on or chase away pollinators and other plant mutualists (Suttle 2003; Dukas 2005; Knight et al. 2005, 2006;
Gonçalves-Souza et al. 2008). On the other hand, carnivores
can indirectly increase plant reproductive output by (i)
decreasing population density of foliar and floral herbivores
(Whitney 2004; Rico-Gray & Oliveira 2007; Romero, Souza
& Vasconcellos-Neto 2008) and ⁄ or (ii) increasing relocation
frequency of winged pollinators and thus the rate of flower
2011 The Authors. Journal of Animal Ecology 2011 British Ecological Society
Contrasting trophic cascades 697
visitation (Altshuler 1999). Therefore, the effects of carnivores on fitness of flowering plants can be context dependent
(e.g. Altshuler 1999, Romero & Vasconcellos-Neto 2004,
Romero, Souza & Vasconcellos-Neto 2008; Hoeksema et al.
2010) and range from strongly negative to strongly positive.
This implies that effects of carnivores on plant–pollinator
and plant–herbivore interactions should not be evaluated in
isolation from each other. Instead, both effects have to be
assessed to evaluate the overall net effect of carnivores on
plant fitness in natural settings where both herbivores and
pollinators occur simultaneously.
Several characteristics of carnivores may affect the
strength and direction of their effects on plant fitness. For
instance, predator’s hunting mode has been shown to affect
predator’s impact on prey behaviour, plant biomass and ecosystem functioning (Schmitz & Suttle 2001; Preisser, Orrock
& Schmitz 2007; Schmitz 2007, 2008). Active hunters (e.g.
birds and ants) forage on both vegetative and reproductive
plant structures and are more likely to come into contact with
(and hence feed more on) relatively sedentary herbivores than
with very mobile and transient pollinators. In contrast,
sit-and-wait predators like crab spiders and lizards usually
forage upon or close to sites of predictably high prey densities
like flowers (Morse 2007) and hence are likely to capture
more pollinators than herbivores. Also, carnivores having
broad habitat domain, i.e. large range of microhabitat use
and high ability to pursue prey, may influence the whole
pollinator community and hence have stronger cascade
effects on plants than carnivores having narrow habitat
domain (Preisser, Orrock & Schmitz 2007; Schmitz 2007).
Furthermore, we predict that parasitoids have stronger
positive effects on plant fitness than predators; this is because
parasitoids are more specialized than other carnivores in
their herbivore host requirements and also because they are
less likely to disrupt plant–pollinator interactions.
Some plants have mutualistic relationships with carnivores
and use them as indirect biotic defences against herbivores
(Heil 2008; Rosumek et al. 2009). In this case, plants usually
provide carnivores with various kinds of rewards (e.g. extrafloral nectaries and domatia), which greatly affect carnivore
densities and activity and, hence, their effect on herbivores
(Rosumek et al. 2009). Therefore, we predict that carnivores
have stronger positive effects on fitness of plants that have
mutualistic interactions with carnivores when compared to
plants that lack any biotic defence.
The majority of studies on carnivore effects on plant fitness
have been conducted in either temperate or tropical climatic
zones. Tropical plants are more prone to be pollen limited
(Larson & Barrett 2000), and the longevity of tropical flowers
is shorter than that of temperate ones (Primack 1985). Therefore, disruption of pollination by carnivores may have more
negative consequences for tropical plants than for temperate
ones. On the other hand, tropical plants suffer more damage
from herbivores than temperate plants (Coley & Barone
1996; Schemske et al. 2009) and hence may be expected to
benefit more from carnivore effects on herbivores. Therefore,
we predict that both the negative and positive cascading
effects of predators on plant fitness are stronger in the tropics.
In this review, we explore the above sources of variation by
conducting a meta-analysis of 67 individual studies on carnivore effects on plant fitness. The main questions addressed
were: (i) What is the overall net magnitude of the carnivore
effect on plant fitness components? (ii) Do predator hunting
mode and habitat domain affect the magnitude or direction
of carnivore effects on plant fitness? (iii) Does the presence of
indirect plant defences and, hence, attractors for carnivores
affect the magnitude and direction of the carnivore effects on
plant fitness? and (iv) Does the strength of the trophic cascades vary between temperate and tropical regions?
Materials and methods
DATA BASE, INCLUSION CRITERIA AND SOURCES OF
VARIATION
The search strategy and the complete data base are presented in the
Appendix S3 (Supporting Information). To be included in our metaanalysis, the papers had to meet the following criteria. First, the study
should have provided a comparison of plant fitness in the presence of
carnivores and under conditions where carnivores were absent or
their density was reduced. To evaluate the effects of carnivores on
plant fitness, we included in our analyses only the estimates from
experiments in which the treatments (presence ⁄ absence of carnivores) were applied to separate plants rather than to individual flowers, inflorescences or flowering stems within the same plant. We made
an exception for ants and included studies comparing effects of ant
presence and absence on different stems within the same plant for the
following reasons: (i) in contrast to other predators that typically forage on a single flower (e.g. crab spiders), ants forage over the whole
plant they have access to; (ii) there was no significant difference
between effects of ants on whole-plant fitness and reproductive output of individual stems within a single plant (Qb = 2Æ6, d.f. = 1,
P = 0Æ305). We included experimental studies that have manipulated carnivore presence or density [either directly, by introducing or
removing carnivores, or indirectly, by removing plant rewards such
as extra-floral nectaries (EFNs)] as well as observational studies conducted in sites where carnivores were naturally present or absent or
present at different densities (gradient studies). In the latter cases, we
only included data from sites with min and max carnivore densities,
as carried out in previous meta-analyses (e.g. Knight et al. 2006). In
the case of observational studies, we designated as control the condition in which predators were absent or occurred at very low density
and as experimental treatment the condition in which predators were
present or occurred at higher density. Second, to be included in our
meta-analysis, studies in the control and experimental groups had to
be carried out simultaneously and using the same plant species.
Third, we considered papers that explicitly investigated the influence
of predators or parasitoids on plant traits that are directly related to
plant fitness. The plant fitness components included were number of
flowers, fruits or seeds per plant or stem and number of seeds per
fruit. If studies reported herbivore damage to seeds and fruits in the
absence and the presence of carnivores, these data were also included
in our meta-analysis, but the sign of the effect () or +) was reversed
(i.e. reduced herbivore damage to fruits and seeds in the presence of
predators indicated positive effect of predators on plant fitness). Data
on plant growth, plant biomass, plant nutrition, seed or fruit
2011 The Authors. Journal of Animal Ecology 2011 British Ecological Society, Journal of Animal Ecology, 80, 696–704
698 G. Q. Romero & J. Koricheva
biomass, or bud and flower damages were not included in our metaanalysis because these measures do not assure that plant fitness is
affected. Fourth, we only included studies on indirect effects of carnivores on plant fitness through trophic cascades via herbivores or pollinators; we disregarded studies in which predators acted as
pollinators or nectar thieves and studies on parasitic castration in
ant-myrmecophyte systems. Finally, to be included, studies had to
report mean fitness estimates for control and experimental treatments, some measure of variation (SD, SE or CI) and sample sizes.
In addition to the estimates of the effects of predators on plant fitness components, we also recorded several study characteristics
(sources of variation). These characteristics included predator hunting mode, predator habitat domain, predator taxa and mechanism of
their effects (via pollinators or via herbivores). Carnivore effects on
plant fitness were classified as mediated via herbivores if the study
compared degrees of seed or fruit damage in the presence and the
absence of herbivores and the authors of the original study explicitly
interpreted the effect as herbivore mediated. Similarly, carnivore
effects were classified as pollinator mediated if the study compared
numbers of undamaged seeds or fruits in the presence and the
absence of carnivores and the authors of the original study explicitly
interpreted the effect as pollinator mediated. Five papers (see Appendix S1, Supporting Information) evaluated both effects via herbivory
and effects via pollinators; these data were generally obtained from
different flowers or inflorescences per plant or using different experimental sets. Carnivore taxa included were spiders, ants, bugs, wasps,
beetles, dragonflies, birds and reptiles (lizards and snakes); we also
included parasitoids (parasitic Hymenoptera) in our analysis. Hunting mode was classified as sit-and-wait (e.g. crab spiders, lizards), sitand-pursue (e.g. lynx spiders) or active hunters (e.g. ants, jumping
spiders, dragonflies, birds, wasps); Appendix S1 (Supporting Information) provides hunting modes for each carnivore species evaluated. Predator habitat domain was classified as narrow for those taxa
that typically forage locally upon foliage or flowers (spiders, beetles,
bugs) and broad for those taxa that forage in relatively large areas
and are not restricted to one or few individual plants (e.g. birds, dragonflies, wasps, ants and reptiles). Parasitoids were excluded from the
analyses of effects of hunting mode and habitat domain because they
are very specialized in their foraging and not comparable in this
respect to carnivores. We also recorded whether the plant species in
question uses carnivores as indirect defences (see Heil 2008) and thus
offers food rewards (floral and EFNs) and other carnivore attractors
(fruit juice and presence of honeydew-producing insects), plant structures used for shelter (domatia) or foraging sites (glandular
trichomes). We defined tropical studies as those undertaken between
the tropics of Cancer and Capricorn. Additional sources of variation
examined (plant habit, predator diversity, system [natural vs. managed], type of study [observational and experimental], length of the
experimental studies and invasive vs native predators) are presented
in the Appendix S4 (Supporting Information).
DATA EXTRACTION FROM STUDIES
Many studies reported more than one estimate of effects of predators
on plant fitness, which may be nonindependent. Nonindependence of
the data may lead to underestimation of the standard error of the
mean effect and thus may inflate significance levels for statistic tests
(see Gurevitch & Hedges 1999; Koricheva 2002). We minimized nonindependence of multiple estimates in our data base as following: (i)
for time series measures, we only included data from the last estimate
to decrease the likelihood of evaluating transient dynamics (cf Schmitz, Hambäck & Beckerman 2000); (ii) independent experiments
reported in the same paper that were conducted in different seasons
or years or in distinct geographical regions were treated as independent comparisons because predators under study migrate relatively
short distances and have short life cycles, and thus, it is likely that
their effects are local and seasonally restricted; (iii) When multiple
response variables (e.g. fruits in different phenophases) were
reported, we considered only those which are most representative for
plant fitness (e.g. fruits in oldest phenophase). The above steps
allowed us to reduce the number of estimates per study to 2Æ4 on average. To avoid violation of the assumption of independence of statistical tests owing to inclusion of multiple estimates per study, we used
the ‘shifting units’ approach recommended by Cooper (1998). First,
to estimate the overall effect of carnivores on plant fitness, we have
conducted meta-analysis using one effect estimate per study calculated as a mean of effect size estimates reported in each study. Second, to analyse sources of variation in the magnitude of the effect, we
have included multiple estimates per study. This allowed us to retain
the maximum information from studies and hence to examine more
sources of variation in the magnitude of the effects. The problem of
nonindependence of multiple comparisons from the same study is
much less severe for the analyses of sources of variation because in
such analyses, multiple estimates of the effect from the single study
are included in different subgroups to be compared, i.e. each study
would contribute only one data point to each of the categories distinguished by the explanatory variable (Cooper 1998).
In addition to multiple effects from the same study, the explanatory variables considered in the meta-analysis may also be nonindependent from each other. Associations among these variables were
tested using G-test (Zar 1996). In the case of significant associations,
effects of each variable on the strength of the response variable were
evaluated separately at each level of the other explanatory variable
(see Koricheva 2002).
Data on means, standard deviations and sample sizes for experimental treatments (carnivores present) and controls (carnivores
absent or at low density) were obtained from texts, tables or graphs.
The graphs were enlarged and saved as JPEG figures and then
imported to ImageJ 1.42q software (http://rsb.info.nih.gov/ij) for
data extractions.
THE META-ANALYSIS
We first converted values of means, standard deviations and sample
sizes of each study to effect sizes and their associated variances to
place the data from primary studies on a common scale (Gurevitch &
Hedges 2001). Here, we estimated the magnitude of carnivore effect
on plant fitness by using log response ratio (ln R), ln R = ln(XE ⁄ XC),
where XE and XC denote mean plant fitness in the presence (or higher
density) and absence (or reduced density) of carnivores, respectively
(Hedges, Gurevitch & Curtis 1999). Positive or negative effects indicate that carnivores increase or decrease plant fitness, respectively.
pffiffiffiffiffiffiffi
The condition for the use of ln R is that the NE XE =SDE and
pffiffiffiffiffiffiffi
NC XC =SDC >3 (Hedges, Gurevitch & Curtis 1999), where N, X
and SD denote, respectively, sample size, mean and standard deviation from experimental (E) or control groups (C). Our data met this
pffiffiffiffiffiffiffi
requirement as 90% of the values of NC XC =SDC and 86% of the
pffiffiffiffiffiffiffi
values of NE XE =SDE were >3. We conducted analyses using ln R
as a measure of effect size and then back transformed ln R to % difference between control and treatment [as (EXP ln R )1) · 100%]
for the ease of interpretation.
To ensure that the results of our meta-analysis are not biased
owing to the choice of ln R as a metric of the effect size, we have also
conducted analyses using standardized difference between the means,
2011 The Authors. Journal of Animal Ecology 2011 British Ecological Society, Journal of Animal Ecology, 80, 696–704
Contrasting trophic cascades 699
0·6
0·4
122
Effect size (ln R)
Plants without attractors
0·2
8
0·0
19
15
–0·2
9
All plants
–0·4
Active hunter
Sit-and-wait
Active hunter
Sit-and-pursue
–0·6
Sit-and-wait
Hedges’d, as metric of the effect size (Hedges & Olkin 1985). The
results of the analysis were the same for both metrics, and therefore,
we report only ln R and corresponding % fitness changes because of
the ease of interpretation and because ln R has been used in previous
meta-analyses on trophic cascades (Schmitz, Hambäck & Beckerman
2000; Shurin et al. 2002; Borer et al. 2005; Knight et al. 2006;
Rosumek et al. 2009).
We used a mixed effects meta-analysis model, which assumes that
there is a random variation among studies within each category of
explanatory variable (e.g. within each type of hunting mode or type
of habitat domain), but variation among categories is fixed (Gurevitch & Hedges 2001). Mixed models are often preferable to fixed
effects models because their assumptions are more likely to be satisfied in ecological data (Gurevitch & Hedges 2001). Ninety-five per
cent confidence intervals (CI) were estimated by bootstrapping based
on 4999 iterations, and the effect sizes were considered significant
when the CI did not overlap with the zero. P values for the betweengroup heterogeneity (Qb) tests were obtained by randomization tests
based on 4999 iterations. The meta-analysis was carried out by using
the MetaWin 2.0 statistical software (Rosenberg, Adams & Gurevitch 2000). Analyses of publication bias are presented in the Appendix S5 (Supporting Information).
Hunting mode
Fig. 1. Effects (mean ln R and 95% CI) of carnivores with different
hunting mode on fitness of plants with and without attractors
together (all plants) and for those without attractors. Sample sizes
are indicated next to the error bars.
Results
The final data base consisted of 163 estimates of effect sizes
from 67 papers or book chapters published in 1967–2009
(Appendices S1 and S2, Supporting Information). Most of
the studies examined effects of invertebrate carnivores (95%
of all comparisons), particularly ants and spiders (79%), and
54% of the studied plants were woody (shrubs, trees, vines).
Seventy-seven per cent of the 163 estimates referred to plants
that had some type of attractors for predators (e.g. EFNs,
domatia, honeydew-producing herbivores and glandular trichomes). Most of the estimates were from studies conducted
in natural field conditions (84%), and the rest of studies were
conducted in agricultural fields, greenhouses and common
gardens (Appendix S1, Supporting Information).
The overall effect of carnivores on plant fitness was positive and significantly different from 0 (analysis based on single mean estimate per study: ln R = 0Æ27, 95% CI = 0Æ14–
0Æ44, n = 67; analysis based on multiple estimates per study:
ln R = 0Æ28, 95% CI = 0Æ19–0Æ37, n = 163); this corresponds to 31–32% increase in plant fitness in the presence of
carnivores. However, total heterogeneity among studies (Qt)
was very high (analysis based on single mean estimate per
study: Qt = 159Æ01, d.f. = 66, P < 0Æ0001; analyses based
on multiple estimates per study: Qt = 443, d.f. = 162,
P < 0Æ0001), indicating that effects varied significantly
among studies, and thus, analysis of explanatory variables is
warranted. The magnitude of the effect did not depend on
the fitness measure used (no. of flowers, fruits and seeds)
(Qb = 3Æ4, d.f. = 3, P = 0Æ683). Therefore, in the rest of the
analyses, we did not differentiate between different fitness
measures. As expected, predators had opposite effects on
plant fitness depending on whether they affected plant mutualists (pollinators) or antagonists (herbivores). When predators interfered in plant–pollinator mutualism, they decreased
plant fitness by 17% (ln R = )0Æ19, 95% CI = )0Æ29 to
)0Æ09, n = 36). In contrast, when predator effects on plant
fitness were mediated by their negative effects on herbivores,
plant fitness was increased by 51% (ln R = 0Æ41, 95%
CI = 0Æ38 to 0Æ60, n = 126). For studies in which both
effects via pollinators and herbivores were evaluated in the
same system (Appendix S1, Supporting Information: Louda
1982, Norment 1988, Altshuler 1999; Romero & VasconcellosNeto 2004, Romero, Souza & Vasconcellos-Neto 2008), the
effect of carnivores on plant fitness via pollinators was nonsignificant (ln R = 0Æ01, 95% CI = )0Æ07 to 0Æ08, n = 10),
but positive and significant via herbivores (ln R = 0Æ40, 95%
CI = 0Æ14–0Æ65, n = 7; Qb = 14Æ2, d.f. = 1, P = 0Æ002).
The overall net effect of carnivores via pollinators and herbivores in these studies was positive and significant (ln
R = 0Æ10, 95% CI = 0Æ0005–0Æ24, n = 17).
Predator hunting mode influenced the strength of the
trophic cascade (Qb = 18Æ8, d.f. = 2, P = 0Æ041). The sitand-wait and sit-and-pursue predators had no significant
effects on plant fitness, whereas the active hunters increased
plant fitness by 36% (Fig. 1). However, the predator hunting
mode was significantly associated with the presence of plant
attractors; sit-and-pursue predators occurred only on plants
with some type of attractors, whereas sit-and-wait predators
and active hunters occurred on both plants with and without
attractors. When we restricted the analysis to plants that had
no attractors for predators, the effect of sit-and-wait and
active hunters became marginally significant and negative
(Fig. 1), and the difference between the two types of predators was nonsignificant (Qb = 0Æ17, d.f. = 1, P = 0Æ706).
To compare the magnitude and direction of the effects for
predators with broad and narrow habitat domains and
among different carnivore taxa, we removed studies on
2011 The Authors. Journal of Animal Ecology 2011 British Ecological Society, Journal of Animal Ecology, 80, 696–704
700 G. Q. Romero & J. Koricheva
3·0
3
3
2·5
Effect size (ln R)
Broad habitat domain
Narrow habitat domain
1·5
3
1·0
0·5
Effect size (ln R)
2
2·0
14
1
2
4
0
30
4
8
6
0·0
12
–1
3
5
2
–0·5
Broad habitat domain
3
plants with attractors from the analysis because carnivore
taxon, domain and presence of attractors were not independent from each other (i.e. vertebrate carnivores and many
predators with broad habitat domain usually occurred on
plants without any attractors; Gdomain vs. attractor = 7Æ08,
d.f. = 1, P = 0Æ008). In addition, habitat domain was not
independent of hunting mode (G = 5Æ32, d.f. = 1,
P = 0Æ021). Therefore, we compared effects of broad vs. narrow habitat domain predators within each type of hunting
mode category. Within the sit-and-wait category, predators
with broad habitat domain decreased plant fitness by 52%,
whereas narrow-domain predators had no significant effect
(Fig. 2; Qb = 14Æ5, d.f. = 1, P = 0Æ013). Within the active
hunting mode, broad-domain predators had significantly
negative effect on plant fitness, whereas narrow-domain predators had significantly positive effect (Fig. 2; Qb = 21Æ5,
d.f. = 1, P = 0Æ002). The broad-domain carnivores
included reptiles, birds, dragonflies, wasps and ants, and all
of them had significant negative effects on plant fitness
(Fig. 3; wasps: ln R = )0Æ53). Narrow-domain carnivores
included spiders, bugs, parasitoids and beetles. While bugs,
beetles and parasitoids had positive effects on plant fitness,
the effects of spiders did not differ from 0 (Fig. 3). Overall,
vertebrates had a strong negative effect decreasing plant fitness by 40%, whereas invertebrates (including parasitoids) in
the absence of attractors increased plant fitness by 33%
(Fig. 3, Qb = 32Æ3, d.f. = 1, P < 0Æ001). Also, parasitoids
had stronger and more positive effects on plant fitness than
predators (Qb = 44Æ9, d.f. = 1, P < 0Æ001): while parasitoids increased plant fitness by 99% (Fig. 3), other carnivores
on average reduced plant fitness by 18%.
Presence and type of plant attractors for carnivores significantly influenced the magnitude and direction of the effects
of predators on plant fitness (Qb = 64Æ3, d.f. = 5,
P < 0Æ001). Predators decreased by 19% fitness of plants
that lacked any attractors (ln R = )0Æ21, 95% CI = )0Æ36
to )0Æ05, n = 24), but increased by 42% fitness of plants that
had attractors (ln R = 0Æ35, 95% CI = 0Æ25–0Æ46,
Invertebrates
Vertebrates
Beetles
Bugs
Spiders
Ants
Parasitoids
Fig. 2. Effects (mean ln R and 95% CI) of carnivores with different
habitat domains and hunting modes on fitness of plants that lack
attractors. Sample sizes are indicated next to the error bars.
Dragonflies
Active hunters
Hunting mode
Birds
Sit-and-wait
Narrow habitat domain
–2
Reptiles
–1·0
Carnivore type
Fig. 3. Effects (mean ln R and 95% CI) of different carnivore taxa on
fitness of plants that lack attractors. Sample sizes are indicated next
to the error bars.
n = 125). When studies on ants (the most commonly studied
predators) were excluded from the analysis, the effects of carnivores on the fitness of plants that have attractors were still
positive (ln R = 0Æ15, 95% CI = 0Æ05–0Æ26, n = 22). When
the effect of carnivores via pollinators was evaluated separately, carnivores had no significant effect on fitness of plants
that had attractors (ln R = 0Æ02, 95% CI = )0Æ08 to 0Æ03,
n = 21), whereas in the absence of attractors, plant fitness
was reduced by 32% (ln R = )0Æ39, 95% CI = )0Æ54 to
)0Æ24, n = 15). As predator taxon was not independent of
the presence and type of plant attractor, we analysed the
influence of plant attractors separately for spiders and ants
because these arthropods were the most representative in our
meta-analysis. When analysis was restricted to studies on spiders, plant fitness was increased by 13% in the presence of
attractors (ln R = 0Æ13, 95% CI = 0Æ03–0Æ23, n = 18), but
the effect did not differ from 0 in the absence of attractors (ln
R = )0Æ13, 95% CI = )0Æ32 to 0Æ006, n = 4). Spiders that
live on plants with EFNs improved plant fitness by 23%,
while spiders that live on plants with glandular trichomes and
on plants with no attractors had no significant effect on plant
fitness (Fig. 4). However, when the effects via pollinators
were removed from the analysis, effects of spiders on the fitness of glandular plants were higher than those on plants
with EFNs, improving plant fitness by 54% (ln R = 0Æ43,
95% CI = 0Æ16–0Æ68, n = 5, Qb = 0Æ004, d.f. = 1, P =
0Æ97). For studies on ants, fitness of plants without attractors
was negatively affected by the predator (ln R = )0Æ13, 95%
CI = )0Æ33 to )0Æ01, n = 4), whereas fitness of plants with
attractors was increased (ln R = 0Æ40, 95% CI = 0Æ29–0Æ54,
n = 103; Qb = 10Æ3, d.f. = 1, P = 0Æ048). Note, however,
that the number of studies without attractors was very small,
and results of this comparison should be interpreted with
caution. There was no statistical difference among different
types of plant attractors (Qb = 8Æ04, d.f. = 2, P = 0Æ177)
2011 The Authors. Journal of Animal Ecology 2011 British Ecological Society, Journal of Animal Ecology, 80, 696–704
Contrasting trophic cascades 701
0·8
Spiders
Ants
Effect size (ln R)
0·6
29
60
0·4
0·2
4
12
14
0·0
Ant-tended insects
Extra-floral nectaries
Reproductive structures
Extra-floral nectaries
Glandular trichomes
–0·2
Attractor type
Fig. 4. Effects (mean ln R and 95% CI) of spiders and ants on plant
fitness in the presence of variable plant attractors. Sample sizes are
indicated next to the error bars.
0·8
0·6
Effect size (ln R)
0·4
Effects on
herbivores
51
Effects on
pollinators
13
71
0·2
0·0
–0·2
23
–0·4
–0·6
Tropical
Temperate
Region
Fig. 5. Effects (mean ln R and 95% CI) of carnivores on plant fitness
via pollinators and herbivores in the tropics and temperate regions.
Sample sizes are indicated next to the error bars.
(Fig. 4). Predatory bugs inhabiting leaf domatia also
improved plant fitness by 23% (ln R = 0Æ21, 95% CI =
0Æ15–0Æ25, n = 4).
The strength of negative effects of predators on plant fitness
via pollination did not differ between the tropics and the temperate regions (Qb = 0Æ11, d.f. = 1, P = 0Æ82). Similarly,
there was no significant difference in predator effects on plant
fitness via herbivory reduction between the tropics and the
temperate zone (Qb = 0Æ16, d.f. = 1, P = 0Æ79) (Fig. 5).
Discussion
Our analyses show that the overall effect of carnivores on
plant fitness depends on the relative effects of carnivores on
plant mutualists (pollinators) and antagonists (herbivores).
In systems where carnivores disrupted plant–pollinator interactions, plant fitness was reduced by 17% in the presence of
carnivores (cf Knight et al. 2006). In contrast, when carnivores affected plants through their effects on herbivores (the
classical trophic cascade), their effect on plant fitness was
positive and stronger than the effect via pollination (51%
increase) (cf Schmitz, Hambäck & Beckerman 2000). Our
meta-analysis has shown for the first time that the overall net
effect of carnivores on plant fitness is positive (32% increase)
and is similar in magnitude or even stronger than previously
reported carnivore effects on plant biomass and herbivory
rate (Schmitz, Hambäck & Beckerman 2000; Shurin et al.
2002; Borer et al. 2005). A similar result (positive effect of
carnivores) emerged when we restricted analysis only to studies in which carnivore effects on plant fitness via pollinators
and herbivores were studied in the same system. Therefore,
our findings add to a growing consensus that trophic cascades are present in terrestrial ecosystems (Schmitz,
Hambäck & Beckerman 2000; Halaj & Wise 2001; Shurin
et al. 2002; Borer et al. 2005; Shurin, Gruner & Hillebrand
2006), although they are weaker than in many aquatic ecosystems (Shurin et al. 2002; Borer et al. 2005; Shurin, Gruner &
Hillebrand 2006). Moreover, the results from the present
study also support our prediction that the strength and direction of terrestrial trophic cascades are strongly influenced by
relative effects of carnivores on pollinators vs. herbivores,
predator hunting mode, carnivore habitat domain and taxonomy, and presence and type of plant attractors.
The net positive effect of carnivores on plant fitness suggests that carnivore effects on herbivores were stronger than
on pollinators. This could be because of several factors. First,
most herbivores are more sessile and remain longer on plants
than pollinators and thus are more vulnerable to carnivores
(e.g. Romero, Souza & Vasconcellos-Neto 2008), while direct
lethal effects of carnivores on pollinators may be less common (Suttle 2003; Morse 2007; Gonçalves-Souza et al. 2008;
Ings & Chittka 2009). Second, many pollinators have welldeveloped sensory systems that allow more detailed assessment of the foraging areas when compared to herbivores
(Gonçalves-Souza et al. 2008; Ings & Chittka 2009; but see
Sendoya, Freitas & Oliveira 2009). Third, plants may be buffered against loss of pollination by attracting different types
of pollinators, some of which are inaccessible to carnivores
(i.e. larger sizes) (Dukas & Morse 2005; Morse 2007). Fourth,
predators (e.g. ants) may increase relocation frequency of
pollinators and thus increase the rate of flower visitation
(Altshuler 1999) and plant fitness. Fifth, stronger effects of
carnivores on herbivores than on pollinators may be an artefact. Only 4 of 17 studies that examined effects of carnivores
on plant fitness via pollinators controlled for herbivore presence or reported that herbivores were absent. If herbivores
that feed on reproductive tissues were present in the majority
of studies that evaluated carnivore–pollinator interactions,
their effects may be underestimated. Positive effects of herbivore removal might have to some extent offset negative
effects of predation on pollinators. We therefore suggest that
2011 The Authors. Journal of Animal Ecology 2011 British Ecological Society, Journal of Animal Ecology, 80, 696–704
702 G. Q. Romero & J. Koricheva
future studies aiming at elucidation of the mechanisms
behind carnivore effects on plant fitness control for herbivore
presence on the plants.
The strength of carnivore effects on plant fitness also
depended on carnivore hunting mode. We expected that cues
from stationary predators (sit-and-wait) could be more indicative of imminent predation risk and thus trigger stronger
negative effects on floral visitors than cues from actively
hunting predators (Preisser, Orrock & Schmitz 2007; Schmitz
2007). In contrast, we found that the effects of sit-and-wait
and sit-and-pursue predators on plant fitness were not significant, whereas active hunters increased plant fitness when
plant attractors were present. Although sit-and-wait predators like crab spiders have been shown to affect pollination
and seed set of individual flowers within the plant (e.g.
Gonçalves-Souza et al. 2008; Brechbühl, Kropf & Bacher
2010), their effects on the whole-plant fitness appear to be
weaker. Plants have various chemical and mechanical strategies to restrict foraging by active hunters (e.g. ants) to foliage
rather than flowers (Willmer et al. 2009), thus reducing negative effects on pollinators. Therefore, our findings do not support our prediction that stationary predators are more prone
to disrupt plant–pollinator mutualism, but instead suggest
that active hunters have more positive effects on plant fitness.
Habitat domain of the predator also significantly affected
the strength of trophic cascades on plant fitness. Predators
with broad habitat domain (e.g. wasps, dragonflies, ants,
birds and reptiles) had negative effects on plant fitness,
whereas the majority of carnivores with narrow habitat
domain had positive effects (Fig. 3). Broad habitat domain
predators typically forage by flying (except ants and reptiles)
and are likely to affect the abundance and behaviour of pollinators, which also reach flowers by flying. In contrast, most
of the narrow-domain carnivores (e.g. bugs, lady birds and
parasitoids) are likely to have stronger effects on herbivores
than on pollinators, and hence, their positive effects outweigh
the negative effects on plant fitness.
Parasitoids increased plant fitness by 99%, whereas predator effects were considerably weaker: 30% increase in plant
fitness in the presence of attractors and 18% reduction in fitness in the absence of plant attractors. Among different predator taxa, only beetles tended to have stronger effects on
plant fitness than parasitoids in the absence of attractors
(Fig. 3). Stronger and more positive effects of parasitoids on
plant fitness may be because of their higher feeding specialization and lack of negative effects on pollinators. Therefore,
parasitoids might be the only guild of carnivores that have no
negative effect on plant fitness.
Some plant species have evolved mutualistic relationships
with carnivores and actively recruit them as indirect defences
against herbivores by providing various rewards in the form
of food (EFN, fruit juices), ‘accommodation’ (domatia) and
foraging sites (glandular trichomes). Although honeydewproducing insects can be costly to the plants, the presence of
such insects may also attract carnivores to the plants and ants
are known to be very protective of the plants bearing colonies
of honeydew-producing insects (Styrsky & Eubanks 2007).
Use of carnivores as indirect plant defences can be effective in
improving plant reproduction (reviews in Heil 2008; Romero
& Benson 2005; Rico-Gray & Oliveira 2007) and is likely to
be the crucial determinant of the direction of the trophic cascades on plant fitness in terrestrial ecosystems. However,
none of the previous meta-analytical studies on trophic cascades (Schmitz, Hambäck & Beckerman 2000; Halaj & Wise
2001; Dyer & Coley 2002; Shurin et al. 2002; Bell, Neill &
Schluter 2003; Borer et al. 2005; Knight et al. 2006) has evaluated the role of indirect plant defences comprehensively. It
has been proposed that plant chemical defences may buffer
trophic cascades in terrestrial ecosystems by dampening
lower interactions (herbivores producers) (see Shurin et al.
2002; Shurin, Gruner & Hillebrand 2006 and references
therein). Here, we showed that indirect defences may have
opposite effect, i.e. they triggered positive trophic cascades
on plant reproduction, whereas the overall magnitude of topdown effects was negative in the absence of them.
While spiders improved plant fitness in the presence of
EFNs, they had no significant effect on fitness of plants with
glandular trichomes. This might be because all the studies on
glandular trichomes evaluated both the costs and benefits of
spiders on plant fitness, while some studies on plants bearing
EFNs evaluated only the positive effects of spiders on plant
fitness via suppression of herbivores and not their potential
negative effects via pollinators. When we excluded effects via
pollination from the analysis, the magnitude of the effects of
spiders on fitness of plants with glandular trichomes (ln
R = 0Æ43) was higher than that of spiders on plants bearing
EFNs (ln R = 0Æ20). Thus, the actual overall effect of EFNs
as mediator of spider–plant mutualisms remains to be investigated. As expected, in the presence of plant attractors, ants
improved plant fitness. The previous meta-analysis by
Rosumek et al. (2009) evaluated only the effects of food
rewards (EFNs, food bodies) on plant reproduction, whereas
we have also evaluated the role of other plant attractors, such
as reproductive structures (e.g. flower, fruit) and presence of
ant-tended insects on plant fitness. While ant effects on plant
fitness were stronger in the presence of ant-tended insects and
EFNs, the presence of reproductive structures had no significant effect. It is possible that by foraging on reproductive
structures (flowers), ants may remove herbivores, but also
chase away pollinators, thus reducing positive effects on
plant fitness. In contrast, although both ant-tended insects
and EFNs may be costly for plants (reviewed in Rutter & Rausher 2004; Styrsky & Eubanks 2007), their costs may be offset by the benefits the ants provide by removing herbivores.
Costs and benefits of plant associations with ants are still
poorly explored and deserve further attention.
Previous meta-analytical studies have shown that the
effects of herbivores on plant biomass, effects of predators on
prey, effects of predators on plant biomass and herbivory
(Dyer & Coley 2002) and biotic defences provided by ants
against herbivory (Rosumek et al. 2009) are all stronger in
the tropics than in temperate regions. We also predicted that
the strength of trophic cascade via both herbivores and pollinators on plant fitness would be stronger in the tropics.
2011 The Authors. Journal of Animal Ecology 2011 British Ecological Society, Journal of Animal Ecology, 80, 696–704
Contrasting trophic cascades 703
However, our analysis showed that the strength of cascading
effects of predators on plant fitness is similar among the tropics and temperate regions. Although tropical plants receive
more herbivory than temperate ones (review in Schemske
et al. 2009), they may be better able to tolerate herbivory or
compensate for it by producing more flowers and seeds after
herbivore attack. In addition, only those plants that are more
pollen limited may have been selected in temperate regions to
test for the trophic cascade of carnivores via pollination.
Thus, other factors not measured here may have influenced
plant reproduction in addition to presence of predators.
interactions on plant reproduction. Finally, although indirect
plant defence has been considered as an important factor in
determining plant fitness (e.g. Heil 2008), to date it has not
been evaluated comprehensively in meta-analyses of terrestrial trophic cascades. Because our study provides evidence
that biotic defences strongly determine the direction of trophic cascades in terrestrial ecosystems, we suggest inclusion
of sources of variation concerning plant defences (chemical,
mechanic and biotic) in future meta-analyses on trophic cascades. Our general understanding of terrestrial systems
would be much improved by including above-mentioned
sources of variation.
CONCLUSIONS AND SUGGESTIONS FOR FUTURE
STUDIES
Acknowledgements
Our meta-analysis evaluated the relative importance of factors that can affect the dynamics of the interactions between
carnivores and plant fitness. We found that cascading effects
of carnivores via herbivores were stronger than via pollinators, which is likely to be because of higher vulnerability of
herbivores to predators or lower sensitivity to predation risk
than pollinators. Details on natural history of pollinators
and herbivores, especially on their avoidance behaviour
against predation risk, are scarce in the literature and could
help understanding the indirect cascade effects of predators
on plant fitness. Comparative studies of predation risk sensitivity of herbivores and pollinators could be valuable. Predator hunting mode (stationary vs. active hunters), habitat
domain and plant indirect defences emerged as important
predictors of predator effects in our analysis. Future empirical studies could investigate simultaneously the indirect
effects of stationary vs. active hunters on the pollinator
behaviours and plant fitness, as well as the contrasting
impacts of predators exhibiting broad vs. narrow habitat
domain on herbivory and pollination. As expected, plant
indirect defences caused strong variation in the strength and
direction of the trophic cascades.
Although we have examined as many studies as possible to
evaluate the contrasting trophic cascades on plant fitness
through pollination and herbivory in terrestrial ecosystems,
the majority of studies were restricted to trophic cascades via
herbivory (75%). Several studies and variables have been
included since a previous meta-analysis on trophic cascade
via pollinators (Knight et al. 2006), but the predator–pollinator–flowering plant interactions are still poorly known.
Moreover, ideally carnivore effects via both pathways (pollinators and herbivores) should be evaluated in the same system. To date, only 5% of studies evaluated both of these
contrasting pathways. Furthermore, for most of the trophic
cascades evaluated here, it is unclear whether the indirect
interactions of carnivores with producers are via consumptive or nonconsumptive effects on prey. In addition, most of
the studies have focused on invertebrate predators and herbivores or pollinators. Although many plants are pollinated by
vertebrates (e.g. hummingbirds), which are vulnerable to
several vertebrate predators (Lima 1991), very few studies
to date evaluated the outcomes of vertebrate–vertebrate
We thank I. Leal, T. Turlings, G. Bernardello, K. Del-Claro and R. Snell for
providing pdfs of their papers and L. Lach and three anonymous reviewers for
the constructive comments on the manuscript. G.Q.R. was supported by
research grants from FAPESP (04 ⁄ 13658-5) and CNPq (309815 ⁄ 2009-6).
References
Altshuler, D.L. (1999) Novel interactions of non-pollinating ants with pollinators and fruit consumers in a tropical forest. Oecologia, 119, 600–606.
Bell, T., Neill, W.E. & Schluter, D. (2003) The effect of temporal scale on the
outcome of trophic cascade experiments. Oecologia, 134, 578–586.
Borer, E.T., Seabloom, E.W., Shurin, J.B., Anderson, K.E., Blanchette, C.A.,
Broitman, B., Cooper, S.D. & Halpern, B.S. (2005) What determines the
strength of a trophic cascade? Ecology, 86, 528–537.
Brechbühl, R., Kropf, C. & Bacher, S. (2010) Impact of flower-dwelling crab
spiders on plant–pollinator mutualisms. Basic and Applied Ecology, 11, 76–
82.
Coley, P.D. & Barone, J.A. (1996) Herbivory and plant defenses in tropical forests. Annual Review of Ecology and Systematics, 27, 305–335.
Cooper, H. (1998). Synthesizing Research: A Guide for Literature Review, 3rd
edn. Sage Publications, Thousand Oaks, CA, 201pp.
Dukas, R. (2005) Bumble bee predators reduce pollinator density and plant fitness. Ecology, 86, 1401–1406.
Dukas, R. & Morse, D.H. (2005) Crab spiders show mixed effects on flowervisiting bees and no effect on plant fitness components. Ecoscience, 12, 244–
247.
Dyer, L.A. & Coley, P.D. (2002) Tritrophic interactions in tropical versus
temperate Communities. Multitrophic Level Interactions (eds T. Tscharntke
& B.A. Hawkins), pp. 67–88. Cambridge University Press, Cambridge,
283pp.
Gonçalves-Souza, T., Omena, P.M., Souza, J.C. & Romero, G.Q. (2008) Traitmediated effects on flowers: artificial spiders deceive pollinators and decrease
plant fitness. Ecology, 89, 2407–2413.
Gurevitch, J. & Hedges, L.V. (1999) Statistical issues in ecological meta-analyses. Ecology, 80, 1142–1149.
Gurevitch, J. & Hedges, L.V. (2001) Meta-analysis: combining the results of
independent experiments. Design and Analysis of Ecological Experiments
(eds S.M. Scheiner & J. Gurevitch), pp. 347–369. Oxford University Press,
New York.
Hairston, N.G., Smith, F.E. & Slobodkin, L.B. (1960) Community structure,
population control, and competition. American Naturalist, 44, 421–425.
Halaj, J. & Wise, D.H. (2001) Terrestrial trophic cascades: how much do they
trickle? American Naturalist, 157, 262–281.
Hedges, L.V., Gurevitch, J. & Curtis, P.S. (1999) The meta-analysis of response
ratios in experimental ecology. Ecology, 80, 1150–1156.
Hedges, L.V. & Olkin, I. (1985) Statistical Methods for Meta-Analysis, Academic Press, Boston, MA.
Heil, M. (2008) Indirect defence via tritrophic interactions. New Phytologist,
178, 41–61.
Hoeksema, J.D., Chaudhary, V.B., Gehring, C.A., Johnson, N.C., Karst, J.,
Koide, R.T., Pringle, A., Zabinski, C., Bever, J.D., Moore, J.C., Wilson,
G.W.T., Klironomos, J.N. & Umbanhowar, J. (2010) A meta-analysis of
context-dependency in plant response to inoculation with mycorrhizal fungi.
Ecology Letters, 13, 394–407.
2011 The Authors. Journal of Animal Ecology 2011 British Ecological Society, Journal of Animal Ecology, 80, 696–704
704 G. Q. Romero & J. Koricheva
Ings, T.C. & Chittka, L. (2009) Predator crypsis enhances behaviourally-mediated indirect effects on plants by altering bumblebee foraging preferences.
Proceedings of the Royal Society B, 276, 2031–2036.
Knight, T.M., McCoy, M.W., Chase, J.M., McCoy, K.A. & Holt, R.D. (2005)
Trophic cascades across ecosystems. Nature, 437, 880–883.
Knight, T.M., Chase, J.M., Hillebrand, H. & Holt, R.D. (2006) Predation on
mutualists can reduce the strength of trophic cascades. Ecology Letters, 9,
1173–1178.
Koricheva, J. (2002) Meta-analysis of sources of variation in fitness costs of
plant antiherbivore defenses. Ecology, 83, 176–190.
Larson, B.M.H. & Barrett, S.C.H. (2000) A comparative analysis of pollen limitation in flowering plants. Biological Journal of the Linnean Society, 69, 503–
520.
Lima, S.L. (1991) Energy, predators and the behavior of feeding hummingbirds. Evolutionary Ecology, 5, 220–230.
Louda, S.M. (1982) Influorescence spider: a cost ⁄ benefit analysis for the host
plant, Haplopappus venetus Blake (Asteraceae). Oecologia, 55, 185–191.
Morse, D.H. (2007) Predator Upon a Flower: Life History and Fitness in a Crab
Spider. Harvard University Press, Cambridge, MA.
Norment, C.J. (1988) The effect of nectar-thieving ants on the reproductive
success of Frasera speciosa (Gentianaceae). American Midland Naturalist,
120, 331–336.
Polis, G.A. (1999) Why are parts of the world green? Multiple factors control
productivity and the distribution of biomass Oikos, 86, 3–15.
Preisser, E.L., Orrock, J.L. & Schmitz, O.J. (2007) Predator hunting mode and
habitat domain alter nonconsumptive effects in predator–prey interactions.
Ecology, 88, 2744–2751.
Primack, R.B. (1985) Longevity of individual flowers. Annual Review of Ecology and Systematics, 16, 15–37.
Rico-Gray, V. & Oliveira, P.S. (2007) The Ecology and Evolution of Ant–Plant
Interactions. The University of Chicago Press, Chicago, IL. 346 pp.
Romero, G.Q. & Benson, W.W. (2005) Biotic interactions of mites, plants and
leaf domatia. Current Opinion in Plant Biology, 8, 436–440.
Romero, G.Q., Souza, J.C. & Vasconcellos-Neto, J. (2008) Antiherbivore protection by mutualistic spiders and the role of plant glandular trichomes.
Ecology, 89, 3105–3115.
Romero, G.Q. & Vasconcellos-Netor, J. (2004) Beneficial effects of flowerdwelling predators on their host plant. Ecology, 85, 446–457.
Rosenberg, M.S., Adams, D.C. & Gurevitch, J. (2000) MetaWin: Statistical
Software for Meta-Analysis. Version 2.0. Sinauer Associates, Inc., Sunderland, MA.
Rosumek, F.B., Silveira, F.A.O., Neves, F.S., Barbosa, N.P.U., Diniz, L., Oki,
Y., Pezzini, F., Fernandes, G.W. & Cornelissen, T. (2009) Ants on plants: a
meta-analysis of the role of ants as plant biotic defenses. Oecologia, 160,
537–549.
Rutter, M.T. & Rausher, M.D. (2004) Natural selection on extrafloral nectar
production in Chamaecrista fasciculata: the costs and benefits of a mutualism
trait. Evolution, 58, 2657–2668.
Schemske, D.W., Mittelbach, G.G., Cornell, H.V., Sobel, J.M. & Roy, K.
(2009) Is there a latitudinal gradient in the importance of biotic interactions?
Annual Review of Ecology, Evolution and Systematics, 40, 245–269.
Schmitz, O.J. (2007) Predator diversity and trophic interactions. Ecology, 88,
2415–2426.
Schmitz, O.J. (2008) Ecosystem function effects of predator hunting mode on
grassland. Science, 319, 952–954.
Schmitz, O.J., Hambäck, P.A. & Beckerman, A.P. (2000) Trophic cascades in
terrestrial systems: a review of the effects of carnivore removal on plants.
American Naturalist, 155, 141–153.
Schmitz, O.J. & Suttle, K.B. (2001) Effects of top predator species on the nature
of indirect effects in an old field food web. Ecology, 82, 2072–2081.
Sendoya, S., Freitas, A.V.L. & Oliveira, P.S. (2009) Egg-laying butterflies distinguish predaceous ants by sight. American Naturalist, 174, 134–140.
Shurin, J.B., Gruner, D.S. & Hillebrand, H. (2006) All wet or dried up? Real
differences between aquatic and terrestrial food webs. Proceedings of the
Royal Society B, 273, 1–9.
Shurin, J.B., Borer, E.T., Seabloom, E.W., Anderson, K., Blanchette, C.A.,
Broitman, B., Cooper, S.D. & Halpern, B.S. (2002) A cross-ecosystem comparison of the strength of trophic cascades. Ecology Letters, 5, 785–791.
Strong, D.R. (1992) Are trophic cascades all wet? Differentiation and donorcontrol in speciose ecosystems. Ecology, 73, 747–754.
Styrsky, J.D. & Eubanks, M.D. (2007) Ecological consequences of interactions
between ants and honeydew-producing insects. Proceedings of the Royal
Society of London B, 274, 151–164.
Suttle, K.B. (2003) Pollinators as mediators of top-down effects on plants. Ecology Letters, 6, 688–694.
Whitney, K.D. (2004) Experimental evidence that both parties benefit in a facultative plant-spider mutualism. Ecology, 85, 1642–1650.
Willmer, P.G., Nuttman, C.V., Raine, N.E., Stone, G.N., Pattrick, J.G., Henson, K., Stillman, P., McIlroy, L., Potts, S.G. & Knudsen, J.T. (2009) Floral
volatiles controlling ant behaviour. Functional Ecology, 23, 888–900.
Zar, J.H. (1996) Biostatistical Analysis. Prentice Hall, Englewood Cliffs, NJ.
662 pp.
Received 3 July 2010; accepted 17 January 2011
Handling Editor: Ben Woodcock
Supporting Information
Additional Supporting Information may be found in the online version of this article.
Appendix S1. Sources of variation and log response ratios of carnivores on plant fitness.
Appendix S2. List of studies used in the analysis.
Appendix S3. The database.
Appendix S4. Additional sources of variation examined.
Appendix S5. Publication bias.
As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials may be
re-organized for online delivery, but are not copy-edited or typeset.
Technical support issues arising from supporting information (other
than missing files) should be addressed to the authors.
2011 The Authors. Journal of Animal Ecology 2011 British Ecological Society, Journal of Animal Ecology, 80, 696–704