Ecology Letters, (2011) 14: 670–676
doi: 10.1111/j.1461-0248.2011.01629.x
LETTER
Indirect plant-mediated interactions among parasitoid larvae
Erik H. Poelman,* Rieta Gols,
Tjeerd A. L. Snoeren, David Muru,
Hans M. Smid and Marcel Dicke
Laboratory of Entomology,
Wageningen University,
P.O. Box 8031, 6700 EH
Wageningen, The Netherlands
*Correspondence: E-mail:
[email protected]
Abstract
Communities are riddled with indirect species interactions and these interactions can be modified by organisms
that are parasitic or symbiotic with one of the indirectly interacting species. By inducing plant responses,
herbivores are well known to alter the plant quality for subsequent feeders. The reduced performance of
herbivores on induced plants cascades into effects on the performance of higher trophic level organisms such
as parasitoids that develop inside herbivores. Parasitoids themselves may also, indirectly, interact with the host
plant by affecting the behaviour and physiology of their herbivorous host. Here, we show that, through their
herbivorous host, larvae of two parasitoid species differentially affect plant phenotypes leading to asymmetric
interactions among parasitoid larvae developing in different hosts that feed on the same plant. Our results show
that temporally separated parasitoid larvae are involved in indirect plant-mediated interactions by a network of
trophic and non-trophic relationships.
Keywords
Competition, Cotesia, induced plant response, parasitoid performance, Pieris rapae.
Ecology Letters (2011) 14: 670–676
INTRODUCTION
Communities are structured by both direct trophic interactions as well
as indirect species interactions. Indirect interactions occur when one
species affects a second species through its effect on the density or
quality of a third species (Ohgushi 2005; Utsumi et al. 2010). For
example, feeding by one herbivore induces changes in morphological
and chemical defence characteristics of plants (Karban & Baldwin
1997; Karban 2011) that negatively and ⁄ or positively affect herbivores
that subsequently feed on the induced plants (Denno et al. 1995;
Agrawal 2000; Ohgushi 2005; Poelman et al. 2008a). Not only do
herbivores induce widely different responses in plants (Heidel &
Baldwin 2004; de Vos et al. 2005), these also differ in their sensitivity
to induced plant responses (Agrawal 2000; Poelman et al. 2008a). Plant
responses to herbivory thereby mediate competition among herbivore
species in which herbivores often affect each other asymmetrically
(Denno et al. 1995; Inbar et al. 1999; Agrawal 2000; Kaplan & Denno
2007). It is now recognized that such indirect plant-mediated species
interactions play a major role in structuring insect communities by
mediating interactions among herbivores, predators and pollinators
(van Zandt & Agrawal 2004; Viswanathan et al. 2005; Kessler &
Halitschke 2007; Ohgushi 2008; Poelman et al. 2008b, 2010; Erb et al.
2011).
Effects of induced plant responses on herbivores may cascade up
the food chain affecting the performance of organisms at higher
trophic levels (Bukovinszky et al. 2009; Gols & Harvey 2009). Such
effects may be most profound for organisms that have an intimate
relationship with their herbivorous prey, such as is found for
parasitoid wasps. Parasitoids are insects that develop inside or on the
bodies of other arthropods, whereas the adults are free-living.
Parasitoid larvae feed on the host tissues and eventually kill their
host (Godfray 1994). For their larval development, parasitoids totally
depend on the resources provided by a single host. Herbivores obtain
nutrition from their food plants. Consequently, parasitoids indirectly
also obtain nutrition from the plant on which their host is feeding
(Bottrell et al. 1998; Ode 2006). Food plant quality has been shown to
2011 Blackwell Publishing Ltd/CNRS
affect the immune response of herbivores to parasitism, and
consequently affect parasitoid survival (Klemola et al. 2007; Karimzadeh & Wright 2008; Bukovinszky et al. 2009; Shikano et al. 2010).
Furthermore, plant secondary metabolites can affect parasitoids
through their herbivorous host (Gols & Harvey 2009).
Herbivore-induced changes in plant chemistry may further depend
on whether the herbivore has been parasitized (Fatouros et al. 2005).
Parasitoid larvae may alter the behaviour and physiology of their
herbivorous host (Brodeur & McNeil 1992) and consequently
parasitized herbivores may induce plant responses that differ from
those induced by unparasitized herbivores. In addition, parasitoids
may alter herbivore–plant interactions in species-specific ways,
resulting in specific changes in plant quality. Such differentially
induced responses by parasitized herbivores may in turn affect
parasitoid larvae developing in another herbivore that is feeding on
the induced plant. And thus, parasitoids may potentially inflict changes
in plant phenotypes through their herbivorous host, which extend to
effects on the performance of parasitoids that develop in another
herbivore on that same plant. As a result, parasitoids may be involved
in an indirect plant-mediated interaction network (Utsumi et al. 2010).
Here, we studied whether this concept of indirect plant-mediated
interactions among parasitoid larvae that develop in temporally
separated herbivores may affect the parasitoid performance (Fig. 1).
Although the concept extends to interactions between parasitoids that
are associated with different species of herbivores, we controlled for
differential induction effects that herbivores themselves have on plant
responses by studying a single herbivore species that is commonly
parasitized by two parasitoid species. We studied the small cabbage
white butterfly, Pieris rapae, that has three generations per year in the
Netherlands and is parasitized by at least two parasitoid species during
each generation (Poelman et al. 2009). Effects of induced responses of
Brassica plants to feeding by P. rapae caterpillars are season wide and
cover the successive generations of the herbivore and its parasitoids
(Poelman et al. 2010). In our experiments, P. rapae caterpillars were
parasitized by either the gregarious endoparasitoid Cotesia glomerata
or the closely related solitary endoparasitoid Cotesia rubecula.
Letter
Plant-mediated interactions among parasitoids 671
reared on P. rapae caterpillars and C. glomerata was reared on P. brassicae.
Cultures of both parasitoid species were reared on their respective
hosts on Brussels sprouts plants, which were maintained in separate
greenhouse compartments (23 ± 1 C, 50–70% RH, 16L : 8D).
At emergence, adult parasitoids were caged in a male-to-female ratio
‡50% and provided with water and honey. Parasitoids were 5 days old
when used to parasitize herbivores providing sufficient time for the
parasitoids to have mated.
Figure 1 Study system of indirect plant-mediated interactions between parasitoids.
The parasitoid larva (P1), while developing in its caterpillar host, affects the
interaction of its caterpillar host (H1) with its food plant. The parasitized herbivore
induces plant traits that affect the spatially and temporally separated larvae of a
second parasitoid (P2) that develops in another caterpillar (H2) on the same food
plant. The schematic illustration follows illustrations of trait-mediated interactions
in Utsumi et al. (2010).
The parasitized herbivores were allowed to feed on Brassica oleracea
plants until the parasitoids had completed their larval development
and had egressed from their host. Thereafter, the plants were infested
for a second time with new P. rapae caterpillars that were parasitized
by one of the two parasitoid species. We assessed the performance of
the two parasitoid species when developing in their herbivorous host
in relation to the status (parasitized or not, parasitoid species) of the
previous P. rapae infestation. We discuss the consequences of indirect
plant-mediated interactions among organisms at the third trophic
level.
MATERIAL AND METHODS
Plants and insects
Seeds of wild B. oleracea originate from the ÔKimmeridgeÕ (508350 N,
28030 E) locality along the south coast of the United Kingdom, near
Swanage in Dorset (Gols et al. 2008). Seeds were germinated and
seedlings were subsequently transferred to 2 L pots containing peat
soil (Lentse potgrond No. 4; Lentse Potgrond BV, Lent, The
Netherlands). Pots were placed in a greenhouse, providing the plants
with a 16 : 8 (light : dark) photoperiod with SON-T light (moles of
quanta; 500 lmol m)2 s)1) (Philips, Eindhoven, The Netherlands) in
addition to daylight, at 18–26 C and 40–70% relative humidity (RH).
When the plants were 4 weeks old, they were fertilized weekly by
applying 100 mL of nutrient solution [Kristalon, Nutritech System,
Moscow, Russia, concentration 3 g L)1, (16N : 6P : 20K : 3Mg)] to
the soil.
Pieris rapae caterpillars were routinely reared on Brussels sprouts
(B. oleracea var. gemmifera cv. Cyrus) plants in a climate room
(20–30 C, 50–70% RH, 16L : 8D). Cotesia rubecula was routinely
Caterpillar treatments
To obtain P. rapae larvae that had developed on the same B. oleracea
accession as used in the experiment, we offered a B. oleracea plant from
the Kimmeridge population to the butterflies in the culture for
oviposition. When the caterpillars were early to mid-second instar
larvae, they were divided into three cohorts, i.e. unparasitized control,
parasitized by C. rubecula, and parasitized by C. glomerata. For parasitism,
mated females of either parasitoid species were individually presented
with single caterpillars and each female was allowed to parasitize up to
10 caterpillars. A caterpillar was considered to be parasitized, when the
female had been observed to insert her ovipositor into the caterpillar.
To test whether these caterpillars indeed contained parasitoid eggs,
24 h after parasitism, we dissected under a stereomicroscope up to
100 caterpillars from the parasitized cohorts used in experiments to
confirm the presence of parasitoid eggs.
Parasitoid performance on plants induced by conspecific and
heterospecific parasitism
To study whether parasitoid performance is affected by changes in
plant quality due to previous herbivory by parasitized caterpillars, we
exposed plants to successive herbivore treatments. Seven-week-old
plants were infested with one of the induction treatments: a full
control of undamaged plants, a control of plants damaged by
unparasitized P. rapae caterpillars, C. glomerata-parasitized caterpillars,
or C. rubecula-parasitized caterpillars. Plants exposed to herbivory were
infested with four parasitized or unparasitized caterpillars per plant.
Plants, 55 per induction treatment, were individually enclosed in
sleeves to prevent herbivores from wandering off the plant. The
caterpillars were allowed to feed on the plants during their entire
immature development or until the parasitoid larvae had egressed. We
removed the parasitoid cocoons and herbivore pupa from the plants.
Three days after the plants had been exposed to one of the four
induction treatments, they were divided into two cohorts of 20 plants
within each induction treatment and subjected to one of the
successive parasitized herbivore treatments. One cohort of plants
was subsequently infested with four caterpillars parasitized by
C. glomerata, the other with six caterpillars parasitized by C. rubecula.
We decided to increase the number of C. rubecula-parasitized
caterpillars to six to obtain sufficient performance data of this
parasitoid for statistical comparison, because we noticed considerable
levels of successful immune responses to parasitoid eggs of the
C. rubecula-parasitized caterpillars used for induction. The parasitized
caterpillars were obtained following the same procedure as for the
induction treatment and we assessed the success of parasitism by
dissection. The parasitized caterpillars were allowed to grow on the
plants until the parasitoid larvae egressed or the caterpillars pupated.
At this point, we monitored the plants daily for parasitoid cocoons,
which were collected and stored in 2.2-mL Eppendorf tubes that were
closed with a piece of cotton wool. The tubes were stored in a climate
2011 Blackwell Publishing Ltd/CNRS
672 E. H. Poelman et al.
cabinet (16L : 8D; 23 C) and we checked the cocoons for emerging
parasitoids daily. We quantified (1) the number of days until cocoons
were formed, (2) the number of days until wasps emerged, (3) cocoon
mass and (4) mortality. We discriminated two events of mortality of
parasitoids. One was caused by mortality of the parasitized caterpillar
before a herbivore pupa or a parasitoid cocoon was formed. The
second event was mortality of the parasitoid by successful development of the caterpillar into a butterfly and was calculated by the
fraction of parasitized caterpillars that yielded a herbivore pupa
instead of a parasitoid cocoon. Because only very few parasitoids did
not emerge from their cocoons, we do not present this third type of
mortality. For the gregarious parasitoid C. glomerata we also quantified
the brood size.
To assess whether the phenotypic differences resulting from the
different induction treatments of the plants affected the performance
of the herbivore itself, we measured the performance of unparasitized
P. rapae when developing on plants that had been exposed to one of
the three induction treatments or on undamaged control plants. Each
plant, 15 plants per treatment, was infested with four caterpillars. The
following performance parameters were measured: (1) number of days
until pupation, (2) pupal mass, (3) number of days until adult
emergence and (4) mortality.
To quantify the differences in the amount of damage caused by the
different caterpillar treatments, we measured the total fresh weight of
leaf material eaten by parasitized and unparasitized caterpillars. Early
second instar caterpillars were either parasitized by C. rubecula or by
C. glomerata or remained unparasitized and were kept individually in
Petri dishes lined with moist filter paper. Every other day the
herbivores were provided with a piece of fresh leaf that had been
weighed on an analytical balance. The remaining leaf tissues after 48 h
of caterpillar feeding were weighed and the amount of leaf tissue
consumed was calculated by subtracting the mass of the partially
consumed leaf from its mass when offered to the caterpillar 2 days
earlier. The weight loss due to desiccation was corrected for by
quantifying this for similarly sized pieces of leaf tissues in Petri dishes
without a caterpillar. This was repeated until the caterpillars pupated
or the parasitoid larvae egressed from their host caterpillar.
Statistical analysis
The amount of fresh leaf tissue consumed by parasitized and
unparasitized caterpillars was analysed with a Kruskal–Wallis test and
post hoc differences were identified using Mann–Whitney U-tests.
Effects of induction by one of the four herbivory treatments
(undamaged, unparasitized P. rapae, or P. rapae parasitized by
C. rubecula or by C. glomerata) on performance parameters of
subsequently feeding unparasitized or parasitized herbivores was
analysed by restricted maximum likelihood (REML) analysis. The
performance parameters (days until cocoon was formed, days until
wasp emerged, cocoon mass, brood size) were each analysed in a
separate REML model including the plant induction treatment as
a fixed factor and as a random factor the parasitoids were nested
within the plant they originated from. The mortality of the parasitoids
and the number of P. rapae that survived parasitism on a plant were
analysed with general linear models (GLM), using a logit link function
on the dependent variable encoded by the number of events (dead
parasitoid or surviving herbivore) out of the fixed total of herbivores
inoculated to individual plants. We used SPSS 15.0 for Windows and
GenStat 13th Edition to perform the statistical tests.
2011 Blackwell Publishing Ltd/CNRS
Letter
RESULTS
Our method of manual parasitism of herbivores was successful as we
found parasitoid eggs in 95% of the caterpillars that were dissected
under a stereomicroscope and originated from the cohorts that
entered the main experiment. For these successfully parasitized
caterpillars, we noticed that some parasitoid eggs were encapsulated by
the caterpillarÕs cellular immune response within 24 h after parasitism.
The amount of feeding damage depended on caterpillar treatment
(Kruskal–Wallis test, v2=36.985, P < 0.001). Pieris rapae caterpillars
that were parasitized by C. glomerata consumed significantly more plant
tissue (1.84 ± 0.47 g fresh weight, mean ± SD) than unparasitized
caterpillars (1.52 ± 0.34 g) (Mann–Whitney U-test, n = 39, P =
0.039). In contrast, caterpillars parasitized by C. rubecula consumed
much lower amounts of leaf tissue (0.34 ± 0.11 g) compared to
unparasitized caterpillars (Mann–Whitney U-test, n = 40, P < 0.001).
Differences in leaf consumption by healthy unparasitized and
parasitized caterpillars can be the result of host-growth regulation
by the parasitoid. For C. rubecula this results in reduced growth as the
caterpillar only has to sustain development of a single parasitoid,
whereas for C. glomerata growth may be enhanced depending on the
brood size (Harvey et al. 1999).
Performance of unparasitized P. rapae
Unparasitized caterpillars of P. rapae that were feeding on undamaged
control plants developed faster than caterpillars that were feeding on
previously damaged plants (Table 1; Fig. 2). Pieris rapae caterpillars
that fed on plants induced by C. glomerata-parasitized caterpillars had
the slowest development compared to all other induction treatments
and differed significantly in their development time from caterpillars
that fed on undamaged control plants (Table 1; Fig. 2). Mortality,
pupal mass and pupa-to-adult development time were not affected by
the induction treatment (Table 1).
Performance of parasitoids developing in P. rapae
When developing in P. rapae on induced plants, C. rubecula was not
significantly affected by induction treatment of the food plant in any
of its performance parameters. In contrast, C. glomerata parasitoid
larvae had 30% higher mortality when their host was feeding on a
plant previously damaged by C. rubecula-parasitized caterpillars than on
a plant previously damaged by C. glomerata-parasitized caterpillars
(Fig. 3). When C. glomerata-parasitized caterpillars were feeding on
plants that were induced by caterpillars parasitized by C. rubecula,
significantly more parasitized caterpillars developed into adult
butterflies instead of parasitoids than was found for other treatments
(parasitoid mortality by herbivore encapsulation, GLM v2 = 15.256,
P = 0.002) (Fig. 3).
DISCUSSION
Our results show that, through their herbivorous host, parasitoid
larvae affect the plant phenotype and thereby interact with parasitoid
larvae that subsequently develop in herbivores on the same plant.
Even more so, different parasitoid species appear to affect each other
asymmetrically. Pieris rapae hosts that were parasitized by the
gregarious parasitoid C. glomerata induced a plant response that
resulted in high survival of conspecific parasitoid larvae developing in
Letter
Plant-mediated interactions among parasitoids 673
Table 1 Performance parameters and its statistical analysis [restricted maximum likelihood analysis (F) and general linear models (Wald v2)] of unparasitized Pieris rapae
caterpillars and the parasitoids Cotesia rubecula and Cotesia glomerata developing in P. rapae when the caterpillars were feeding on induced plants damaged by primary herbivory of
unparasitized P. rapae caterpillars, or P. rapae caterpillars parasitized by either C. rubecula or C. glomerata (d.f. = 3)
P. rapae parasitized by
Undamaged control
P. rapae
Mortality
Days until pupation
Days until emerged
Mass of pupa (mg)
C. rubecula
Mortality
Days until pupation
Days until adult emerged
Mass of cocoon (mg)
C. glomerata
Mortality
Days until pupation
Days until adult emerged
Clutch size
Mass of single cocoon (mg)
P. rapae
C. rubecula
F
C. glomerata
30%
19.39
26.59
179.94
(18 ⁄ 60)
(0.31)
(0.38)
(2.54)
32%
20.90
27.84
174.37
(19 ⁄ 60)
(0.47)
(0.53)
(3.44)
27%
19.98
27.09
177.51
(16 ⁄ 60)
(0.35)
(0.37)
(3.03)
35%
21.23
27.45
176.85
(21 ⁄ 60)
(0.63)
(0.44)
(3.71)
3.74
0.73
0.39
56%
17.70
23.64
5.79
(67 ⁄ 120)
(0.38)
(0.37)
(0.11)
59%
17.92
24.02
5.76
(71 ⁄ 120)
(0.28)
(0.25)
(0.10)
63%
17.31
23.03
5.64
(76 ⁄ 120)
(0.34)
(0.37)
(0.14)
51%
16.88
22.58
5.73
(61 ⁄ 120)
(0.26)
(0.28)
(0.10)
1.77
1.01
1.20
59%
24.61
29.42
21.96
3.26
(47 ⁄ 80)
(0.40)
(0.38)
(1.71)
(0.12)
50%
25.50
30.83
23.08
3.47
(40 ⁄ 80)
(0.38)
(0.40)
(1.74)
(0.13)
71%
25.92
31.10
22.10
3.22
(57 ⁄ 80)
(0.85)
(0.82)
(1.33)
(0.14)
40%
25.41
30.44
26.07
3.22
(32 ⁄ 80)
(0.46)
(0.44)
(1.80)
(0.09)
1.09
2.12
1.38
1.30
v2
P
1.012
0.798
0.012
0.540
0.760
4.091
0.252
0.163
0.395
0.320
16.486
0.001
0.363
0.112
0.263
0.289
Values present mean (SD).
Boldface type numbers represent significant effects at P < 0.05.
Figure 2 Larval development until pupation of Pieris rapae caterpillars on plants that
had been previously exposed to different herbivore ⁄ induction treatments;
undamaged control plants (white), unparasitized P. rapae caterpillars (black),
caterpillars parasitized by Cotesia rubecula (light grey), or caterpillars parasitized by
Cotesia glomerata (dark grey). Letters above bars indicate statistical grouping based on
post hoc Tukey tests (a = 0.05).
other caterpillars feeding later on the same plant. In contrast, when
C. glomerata developed in hosts feeding on plants that had been
induced by feeding of caterpillars parasitized by C. rubecula, the
parasitoids had a 30% higher mortality. Survival of C. rubecula itself
was not affected by previous herbivory by parasitized or unparasitized
caterpillars.
The difference in survival of C. glomerata was caused by effects of
the induced plant phenotype on the ability of herbivores to mount
their immune response to parasitism. All induction treatments resulted
in similar host mortality ratios, but parasitoids that developed inside
the surviving hosts differed in their success of development. A large
proportion of parasitized herbivores developed into healthy butterflies
and this share was affected by the induction treatment. Herbivory by
caterpillars of P. rapae induces an array of responses in Brassicaceous
plants (van Poecke et al. 2001; de Vos et al. 2005; Broekgaarden et al.
2007). The phenotypic changes following Pieris herbivory in B. oleracea
include morphological changes, altered composition of primary
metabolites, compounds that impair digestibility of leaf tissue, volatiles
and glucosinolate composition (van Poecke et al. 2001; Broekgaarden
et al. 2007; Gols et al. 2008). Glucosinolates, which are secondary
metabolites characteristic for the Brassicaceae family, are produced in
larger concentrations upon caterpillar damage and negatively affect the
development of P. rapae and its parasitoids (Gols & Harvey 2009;
Hopkins et al. 2009). The response of plants to caterpillar feeding is
dependent on the amount of feeding damage as well as the
composition of elicitors that are found in the regurgitant of the
caterpillars (Mattiacci et al. 1995; Mithofer et al. 2005; Bonaventure
et al. 2011). An increase in feeding damage and the presence of
elicitors in the regurgitant of caterpillars both enhance the degree
of induction in the plants, resulting in leaf tissue that contains higher
concentrations of defensive compounds. Even though the performance of healthy P. rapae could be explained by differences in feeding
damage induced by host treatment (P. rapae performed better on
plants induced by host treatments that resulted in reduced feeding),
differences in feeding could not explain parasitoid performance.
In addition to quantitative effects, parasitism also affects the
composition of the regurgitant of Pieris caterpillars (Fatouros et al.
2005). The combined effect of the plantÕs response to levels of
damage and regurgitant composition could explain the effects of
differences in plant quality. Moreover, healthy hosts and parasitized
hosts may differ in their sensitivity to differences in plant quality. For
example, feeding on poor quality food, i.e. food with low nutrient
levels or high concentrations of secondary metabolites, impairs the
immune response of the herbivore to parasitism (Brodeur & Vet 1995;
Kraaijeveld et al. 2001; Karimzadeh & Wright 2008; Bukovinszky et al.
2009). Induced responses of B. oleracea by P. rapae feeding have been
shown to result in significant reduction of the herbivoreÕs cellular
immune response to parasitism (Bukovinszky et al. 2009). On induced
plants, P. rapae encapsulated with its cellular response fewer
2011 Blackwell Publishing Ltd/CNRS
674 E. H. Poelman et al.
Letter
Figure 3 Mortality of Cotesia rubecula (left) and Cotesia glomerata (right) in their herbivorous host Pieris rapae that fed on control (white bars) or induced Brassica oleracea (grey and
black bars). Within bars, the diagonally striped pattern indicates the percentage of dead caterpillars and the remainder of the bar indicates the percentage of parasitoid mortality
due to successful immune responses by herbivores (representing collected herbivore pupa). Letters above bars indicate statistical grouping based on post hoc Tukey tests
(a = 0.05).
C. glomerata eggs than on undamaged control plants, leading to higher
survival of parasitoids on host plants of poor quality (Bukovinszky
et al. 2009).
Effects of parasitic or symbiotic organisms on their host extend the
phenotype of the host. Such extended phenotypes have been shown
to be present at various levels of communities, and have been shown
to affect interactions of the host with other species. In grasses such as
Lolium perenne and Festuca arizonica, symbiotic fungal endophytes
(Neotyphodium) produce alkaloids that enhance the defensive chemistry
of the grasses to herbivore attack. Grasses that had the established
symbiotic interaction had lower herbivore abundance and altered
arthropod community composition from plants that lack endophytes
(Omacini et al. 2001; Faeth & Shochat 2010). Due to the endophyteenhanced levels of defensive chemistry, the reduced leaf intake of the
herbivores also reduced the susceptibility of the herbivores to
baculoviruses (Bixby & Potter 2010). The baculoviruses in turn, are
known to affect the behaviour, such as movement, of the herbivore
(Kamita et al. 1995), that thereby may interact differently with the
plant it is feeding from. Similarly, herbivores that share their food plant
may affect interactions of herbivores with their viruses. In milkweed,
leaf quality is reduced by aphid infestation and the reduced leaf quality
enhances virus transmission and virulence to caterpillars of the
monarch butterfly (de Roode et al. 2011). Thus, not only do indirect
plant-mediated species interactions affect host–parasite interactions,
symbionts or parasites themselves affect interactions of their host with
other species through the extended phenotype of their host resulting
in complex indirect interaction networks.
Although we show here that in such a network parasitoid species
differentially affect plant phenotypes through their herbivorous host
and thereby significantly affect the performance of parasitoids that
subsequently develop in herbivores on the same plant, the significance
of this interaction in selection on parasitoid life histories is difficult to
assess. The two parasitoids studied here are involved in exploitative
competition for host herbivores and in intrinsic competition when
larvae end up in the same herbivore host (Geervliet et al. 2000). Cotesia
glomerata is an inferior larval competitor to C. rubecula (Geervliet et al.
2000). In addition, C. glomerata accepts other Pieris species in its host
range, offering an escape from intrinsic competition with the P. rapae
specialist C. rubecula (Geervliet et al. 2000). Therefore, responses of
C. glomerata to plants induced by C. rubecula-parasitized caterpillars may
2011 Blackwell Publishing Ltd/CNRS
have evolved with confounding factors of both intrinsic competition
and the enhanced mortality by the plant-mediated interaction network
presented here. Cotesia glomerata has been found to avoid plants that
are damaged by caterpillars in which larvae of C. rubecula develop
(Fatouros et al. 2005), which may have been selected by its inferior
larval competitiveness on its own. Nevertheless, here we show that
C. rubecula-parasitized caterpillars also decrease the survival of
C. glomerata when they develop in other caterpillars on that same
host plant, further selecting for avoidance of those host plants by
C. glomerata. Furthermore, C. glomerata does not avoid plants damaged
by caterpillars containing conspecific larvae (Fatouros et al. 2005),
which we here show even to have a positive effect on the survival of
C. glomerata mediated through the host plant.
Our data show that through their herbivorous host, parasitoid
larvae affect plant quality and thereby the survival of parasitoid larvae
that subsequently develop in herbivores feeding on the same plant.
Theoretically, these indirect plant-mediated interactions between
parasitoids may extend to parasitoid species that are parasitizing
different herbivore species and will never be involved in direct
competition due to their host range. Future studies should identify
how parasitoids alter the interaction of their herbivorous host with the
plant, for example by providing an analysis on regurgitant composition of parasitized and unparasitized herbivores, and should address
the scope of indirect plant-mediated interactions between parasitoids
across different herbivore species. Our study contributes to the
awareness that intimate relationships of two species, such as parasitic
or symbiotic interactions, result in extended phenotypes that are
involved in novel interactions with other community members. These
interactions may result in interaction networks that connect species
that seem unrelated based on direct trophic relationships and thereby
may play a profound role in community structure.
ACKNOWLEDGEMENTS
We thank three anonymous reviewers for their constructive comments
on an earlier version of the manuscript; Leon Westerd, André Gidding
and Frans van Aggelen for rearing of the insects and Unifarm for
maintenance of the plants in the greenhouse. We acknowledge the
Earth and Life Sciences Council of the Netherlands Organisation for
Scientific Research (NWO-ALW) for financial support.
Letter
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Letter
Editor, Tim Benton
Manuscript received 27 January 2011
First decision made 24 February 2011
Manuscript accepted 18 April 2011