3. efecto de hma sobre la abundancia de insectos foliares ueda2013
TRANSCRIPT
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O R I G I N A L R E S E A R C H P A P E R
Effects of arbuscular mycorrhizal fungi on the abundanceof foliar-feeding insects and their natural enemy
Koji Ueda • Keitaro Tawaraya • Hideki Murayama • Satoru Sato •
Takashi Nishizawa • Tomonobu Toyomasu • Tetsuya Murayama •
Shinpei Shiozawa • Hironori Yasuda
Received: 2 October 2012 / Accepted: 12 December 2012 / Published online: 17 January 2013
The Japanese Society of Applied Entomology and Zoology 2013
Abstract We investigated the effects of symbiotic asso-
ciation between a plant and an arbuscular mycorrhizalfungus (AMF) on the abundance of aboveground foliar-
feeding insects that differed in feeding mode and their
predator. We examined effects on insect abundance as the
result of AMF-related changes in the quality and quantity of
plants in the field. The numbers of three insects with dif-
ferent foliar-feeding mode (phloem feeder, chewer, and
cell-content feeder) and their generalist predator Orius
sauteri Poppius on soybean Glycine max (L.) Merrill with
and without the AMF Gigaspora margarita Becker & Hall
were compared over time. Symbiotic association between
the AMF and the soybean increased shoot biomass, the
concentration of phosphorus in the soybean, and the abun-
dance of the phloem feeder Aulacorthum solani Kaltenbach,
but did not affect the abundance of generalist chewers. In
addition, the effects of the symbiotic association on the
abundance of cell-content feeding Thrips spp. and the
generalist predator O. sauteri differed between sample
dates. These results indicated that the effects of the sym-
biotic association on the number of foliar-feeding insects
depended on feeding mode and the number of predators.
Keywords Multitrophic interactions Arbuscular
mycorrhiza Foliar-feeding insects Feeding mode
Predacious insect
Introduction
Changes in quality and quantity of terrestrial plants
induced by belowground organisms can affect above-
ground multitrophic interactions (van der Putten et al.
2001). Arbuscular mycorrhizal fungi (AMF), which are
symbiotic belowground microbes, ubiquitously form sym-
biotic associations with the roots of most terrestrial plants
(Hodge 2000). In most cases, AMF improve plant growth
and nutritional status (foliar chemistry) by increasing the
acquisition of such soil nutrients as phosphate (Smith and
Read 2008). Consequently, AMF also affect the abundance
of aboveground organisms, for example herbivorous
insects and their natural enemies (Hartley and Gange
2009).
AMF-induced changes in plant traits are well known to
affect the performance of aboveground herbivorous insects,
but such effects may vary from positive to negative
(reviewed by Gehring and Whitham 2002; Gange 2007;
Gehring and Bennett 2009). For instance, some studies
have shown that AMF increased the growth, fecundity, and
survival of herbivorous insects (Gange and West 1994;
Borowicz 1997; Gange et al. 1999; Goverde et al. 2000)
whereas other studies revealed AMF reduced the growth
and survival of herbivorous insects (Rabin and Pacovsky
1985; Gange and West 1994; Vicari et al. 2002). These
different effects of AMF on herbivorous insects probably
depend on the insects’ feeding mode and host range. Gange
et al. (2002) suggested that AMF negatively affected
generalist chewers but positively affected specialist chew-
ers and sap-suckers feeding on plant phloem (phloem
feeders). Little is known, however, about the effect of AMF
on sap-suckers feeding on plant cell contents (cell-content
feeders), for example thrips (except Koschier et al. 2007).
Because generalist chewers feed on plant cell contents, it is
K. Ueda (&)
The United Graduate School of Agricultural Sciences,
Iwate University, Morioka, Iwate 020-8550, Japan
e-mail: [email protected]
K. Tawaraya H. Murayama S. Sato T. Nishizawa
T. Toyomasu T. Murayama S. Shiozawa H. Yasuda
Faculty of Agriculture, Yamagata University,
Tsuruoka, Yamagata 997-8555, Japan
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DOI 10.1007/s13355-012-0155-1
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likely that AMF negatively affect the cell-content feeders,
for example thrips (Koricheva et al. 2009). However, most
of these studies have been conducted in the laboratory
(reviewed by Gehring and Whitham 2002) rather than in
the field.
In addition, some studies have revealed that AMF also
indirectly affected abundance and performance of organisms
at higher trophic levels, for example parasitoids, by increas-ingplantbiomass (Gangeet al.2003; Hempel etal. 2009).For
instance, Gange et al. (2003) reported that the incidence of
parasitoid attack on the host insect was affected by the extent
of symbiotic AMF–plant associations in the field. However,
little is known about the effects of AMF on the abundance of
foliar-feeding insects with different feeding modes and on
their predators under field conditions.
In this study we examined the effects of symbiotic
associations between the AMF Gigaspora margarita
Becker & Hall and soybeans Glycine max (L.) Merrill on
the abundance of aboveground foliar-feeding insects and
their predator in the field. We hypothesized that AMFwould affect the abundance of the generalist chewers and
cell-content feeders negatively but generalist phloem
feeders positively, and as a result the abundance of the
generalist predator would depend on prey abundance. To
test this hypothesis, we compared the abundance of gen-
eralist insects with three different foliar-feeding modes
(phloem feeding versus chewing and cell-content feeding)
and their generalist predator on the plants with and without
AMF over time.
Materials and methods
Study insects
We focused mainly on four herbivorous insects and a
predatory bug because of their abundance. The glasshouse-
potato aphid Aulacorthum solani Kaltenbach (Hemiptera:
Aphididae) is a generalist sap-sucking aphid that feeds on
many crops, for example potato and soybean (Nakata 1995;
Takada et al. 2006). Adults and nymphs of the aphids feed
on phloem sap, inserting a stylet in phloem tissues and
sucking out the sap. In addition, we observed individuals of
at least two species of thrips, almost all of which belonged
to Thrips spp. Therefore, thrips are referred to hereafter
simply as Thrips spp. Most folivorous thrips on soybeans in
Japan are generalist cell-content feeders (Kudo 2003).
Adults and larvae of thrips feed on the foliar surface,
piercing surface tissues and sucking out the exuded plant
juices. The bean webworm Pleuroptya ruralis Scopoli
(Lepidoptera: Crambidae) is a generalist chewing moth
whose larvae feed on leaves of nettles and legumes (Motida
2003a). The larvae live inside shelters constructed by
rolling whole leaves. The mugwort looper Ascotis selena-
ria Denis et Schiffermüller (Lepidoptera: Geometridae) is a
generalist chewing moth whose larvae feed on many crops,
for example tea, soybean, and eggplant (Motida 2003b).
Orius sauteri Poppius (Hemiptera: Anthocoridae) is a
generalist predator that preys on several herbivorous
insects, for example aphids and thrips (Nakata 1995;
Mochizuki and Yano 2007).
Design of experiment
This study was conducted in 2006 on the field site of
Kushibiki-machi (38660N, 139930E) in Tsuruoka City,
Yamagata Prefecture, Japan. The study site (25 m 9 55 m)
was treated with a weed killer in early May and rotovated
on 1 July. The soil fumigant dazomet kills such microor-
ganisms as AMF (Thingstrup et al. 1998; Mark and Cas-
sells 1999). We used dazomet to kill microorganisms in all
treatments. Ten plots, each 5 m 9 5 m and separated by
5 m, were established in five blocks, each with a pair of plots. Each plot was fumigated with 950 g Basamid (con-
taining 98 % dazomet; Agro-Kanesho, Tokyo, Japan), after
which each plot was covered with a plastic sheet for
1 week. Before transplanting the soybeans, we confirmed
that no gas residue remained in the soil by using lettuce
seeds in germination tests in each plot. One plot in each
block thereafter was randomly assigned to receive one of
two treatments:
1. non-mycorrhizal plants (-M); and
2. mycorrhizal plants (?M).
The second plot in each block received the other
treatment.
In this experiment, we did not inoculate the soybean
plants with rhizobia, although soybeans are well known to
have symbiotic associations with rhizobia. To inoculate the
soybean with AMF, instead, soil was collected from the
experimental field, and steam-sterilized twice at 80 C for
45 min. Next, 400 g of steam-sterilized soil was mixed
with 1.92 g ammonium sulfate (containing 17 % N),
0.53 g calcium superphosphate (containing 21 % P2O5),
0.74 g potassium sulfate (containing 20 % K 2O), and
1.92 g calcium carbonate as a pH regulator. Two hundred
fifty plastic pots (12 cm in diameter and 9 cm in depth)
were each filled with the soil. Half of these pots also each
received 2 g G. margarita, which was purchased as a
commercial inoculum from Central Glass (Tokyo, Japan).
Seeds of the soybean (cv. Suzuyutaka) were sown on 27
May. Plants were grown in an environmentally controlled
glass chamber (70 % relative humidity (RH), natural light
condition, and 20 C). All seedlings (24 or 25 seedlings per
plot) were transplanted from the pots into each plot in five
rows at intervals of 60 cm, 33 days after sowing.
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The numbers of individuals of A. solani, Thrips spp.,
P. ruralis, A. selenaria, and O. sauteri on 5 randomly
selected plants per plot were counted 18 and 47 days after
transplanting (DAT). The total number of each insect on 5
plants combined, per plot, was used for analysis.
Shoot biomass, shoot phosphorus concentration,
and arbuscular mycorrhizal colonization
Three plants per plot were randomly sampled 35 DAT and
separated into shoot and root. The shoots were oven-dried
at 70 C for 48 h and then weighed. Ground shoots were
digested with HNO3–HClO4–H2SO4 solution. Phosphorus
concentration in the digested solution was determined
colorimetrically by means of the vanado molybdate yellow
assay (Olsen and Sommers 1982). Phosphorus content was
determined by multiplying dry shoot biomass by phos-
phorus concentration. These plant traits of three plants per
plot were averaged to avoid pseudoreplication.
To estimate the percentage of mycorrhizal colonizationof the roots of the soybeans, all of the root samples were
boiled in 10 % KOH solution at 80 C for 5 min before
staining with 0.05 % aniline blue in 70 % glycerol solution
at 80 C for 5 min. These roots were observed under a
compound microscope at 100 or 2009 magnification. The
percentage of the root colonized was determined by the
grid-line intersect method (Giovannetti and Mosse 1980).
Statistical analysis
All analysis was performed with R (version 2.15.1 for
Windows). To examine the effects of the AMF on the dry
weight biomass of the soybeans, phosphorus concentrations,
and phosphorus content, we used a generalized linear mixed
model (GLMM) with a normal distribution and an identity
link function (lmer function in the lme4 package; maximum
likelihood estimation). AMF were regarded as fixed effects,
and block as random effects. The significance of fixed effects
in GLMM was assessed by use of likelihood ratio tests.
To examine the effects of AMF and sample dates (18DAT
and 47DAT) on the abundance of A. solani, Thrips spp., and
O. sauteri on soybeans, we used GLMM with a Poisson dis-
tribution and a log link function (Laplace approximation).
AMF and sample dates were regarded as fixed effects, and
blocksand plots as random effects. However, the abundance of
P. ruralis and A. selenaria was only used 47 DAT, because
only a single individual of P. ruralis was recorded on -M
plants and A. selenaria was not observed 18 DAT. Model
comparisons were conducted by use of likelihood ratio tests(Zuur et al. 2009).
A generalized linear model (GLM) with a Poisson dis-
tribution and a log link function was used to test whether
AMF, the abundances of A. solani, and Thrips spp. affected
the abundance of O. sauteri. Overdispersion was resolved
by use of a quasi-Poisson distribution. Model comparisons
were conducted using likelihood ratio tests (Poisson) or
F -tests (quasi-Poisson) (Zuur et al. 2009).
Results
The percentages of mycorrhizal colonization of ?M and -M
plants on the transplanting day were 13 ± 6 % and 0 %,
respectively, and 26 ± 5 % and 0 % on 35 DAT (Table 1).
The shoot biomass of ?M plants was significantly greater than
that of -M plants (Table 1). The phosphorus concentration
of ?M plants was marginally significantly greater than that of
-M plants (Table 1). The phosphorus content of ?M plants
was significantly greater than that of -M plants (Table 1).
The abundance of A. solani was significantly higher on
?M plants than on -M plants (Table 2; Fig. 1). The
abundance of Thrips spp. was marginally significantly
higher on ?M plants than on -M plants (Table 2; Fig. 1).
In addition, the abundance of A. solani and Thrips spp.
were significantly higher 47 DAT than 18 DAT (Table 2;
Fig. 1). There was a significant interaction between the
effects of AMF and sample date on the abundance of
Thrips spp. (Table 2; Fig. 1). AMF did not significantly
affect the abundance of P. ruralis and A. selenaria
(Table 2; Fig. 1). AMF did not significantly affect the
abundance of O. sauteri (Table 2; Fig. 1). The abundance
of O. sauteri was significantly higher 47 DAT than 18 DAT
Table 1 Arbuscular mycorrhizal colonization, shoot biomass, shoot phosphorus concentration, and shoot phosphorus content of soybean plants
inoculated with or without Gigaspora margarita 35 days after transplanting (mean ± SE)
Treatment Colonization (%) Shoot biomass (g/plant) Phosphorus concentration (mg/g) Phosphorus content (mg/plant)
-M 0 5.28 ± 1.72 1.19 ± 0.29 8.16 ± 4.42
?M 26 ± 5 10.56 ± 1.30 1.98 ± 0.34 20.06 ± 2.76
df 1 1 1
v2
5.62 3.63 5.16
P 0.018 0.057 0.023
Statistics are based on GLMM with block as random effect
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(Table 2; Fig. 1). There was a marginally significant
interaction between the effects of AMF and sample date onthe abundance of O. sauteri (Table 2; Fig. 1).
GLM showed that there was a marginally significant
effect of the abundance of Thrips spp. on the abundance of
O. sauteri 18 DAT (df = 8, Z = 1.83, P = 0.067). In
addition, there was a significant effect of the abundance of
Thrips spp. on the abundance of O. sauteri on plants 47
DAT (df = 8, t = 3.56, P = 0.007). These results indicate
that the abundance of O. sauteri increased with increasing
the abundance of Thrips spp. (Fig. 2).
Discussion
This study demonstrated that symbiotic association
between the AMF and the soybean increased shoot biomass
and phosphorus concentration of the soybean and the
abundance of the phloem feeder A. solani, but did not
affect the abundance of generalist chewers P. ruralis and
A. selenaria. In addition, the effects of the symbiotic
association on the abundance of cell-content feeding Thrips
spp. and the generalist predator O. sauteri differed between
sample dates. The effects of the symbiotic association on
Table 2 Results of GLMM
with block and plot as random
effects, for the abundance of
herbivorous insects and their
predator on soybean plants
inoculated with or without
Gigaspora margarita 18 and
47 days after transplanting
Response variable Explanatory fixed variable Estimate SE Z P
Aulacorthum solani Intercept -1.53 0.64 -2.39 0.017
AMF 2.97 0.68 4.38 \0.001
Sample date 1.04 0.23 4.48 \0.001
Thrips spp. Intercept 3.69 0.33 11.11 \0.001
AMF 0.91 0.47 1.96 0.051
Sample date 2.58 0.06 40.25 \0.001
AMF 9 sample date -1.18 0.08 -15.02 \0.001
Pleuroptya ruralis Intercept 1.16 0.25 4.65 \0.001
AMF -0.21 0.37 -0.56 0.578
Ascotis selenaria Intercept -0.22 0.5 -0.45 0.655
AMF 0.56 0.63 0.89 0.372
Orius sauteri Intercept -2.02 1.07 -1.89 0.059
AMF 2.07 1.16 1.78 0.076
Sample date 3.74 1.02 3.68 \0.001
AMF 9 sample date -2.16 1.11 -1.95 0.052
Fig. 1 The abundance of herbivorous insects and their
predator on soybean plants with
or without AMF (?M or -M, as
represented by closed and open
circles, respectively) 18 and
47 days after transplanting
(DAT). Error bars indicate SE
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the number of foliar-feeding insects depended on feeding
mode.
The soil fumigant dazomet was very effective at killing
native AMF in the field. The percentages of mycorrhizal
colonization of soybeans that were sampled 35 DAT,
however, were similar to those in previous field experi-
ments (Vejsadová et al. 1992; Sanginga et al. 1999). These
results suggest that dazomet did not negatively affect the
symbiotic associations of soybeans with the AMF after
inoculated plants were transplanted into the field plots.
Several hypotheses have been proposed to explain
how AMF affect plant–herbivore interactions. Gange
et al. (2002) suggested that AMF positively affected the
growth of phloem feeders but negatively affected the
larval performance of generalist chewers feeding on plant
cells. AMF may positively affect the growth of phloem
feeders by enlarging the vascular bundle, making the
phloem elements more accessible; as a result AMF
increase the fecundity of phloem feeders (Gange et al.
1999). AMF may negatively affect the growth of
generalist chewers that feed on plant cells by stimulating
increased plant chemical defense (Gange and West 1994;
Gange et al. 2002). Chewers feeding on cell contents
generally are susceptible to the presence of secondary
metabolites, which are commonly stored inside cells
(Larsson 1989).
Some studies have shown that AMF increased the
growth and fecundity of phloem-feeding aphids (Gangeand West 1994; Gange et al. 1999). For example, Gange
et al. (1999) found that AMF-infected plants supported
increased adult weight, growth rate, and fecundity of the
two aphids Myzus persicae Sulzer and M. ascalonicus
Doncaster. Similarly, in this study, AMF increased the
abundance of phloem feeder A. solani. This result is con-
sistent with the hypothesis that sap-suckers feeding on
plant phloem are positively affected by AMF (Gange et al.
2002).
Thrips feed on plant cell contents, but the effect of AMF
infection of host plants on the abundance of such insects
feeding on cell contents is poorly understood (but seeKoschier et al. 2007). Hoffmann et al. (2009) reported
greater oviposition by the two-spotted mite Tetranychus
urticae Koch (a cell-content feeder) on AMF-infected
plants, suggesting that increased phosphorus concentration
because of AMF positively affected their population
growth. In addition, Chen et al. (2004) found that the high
plant-phosphorus concentration increased the abundance of
the western flower thrips Frankliniella occidentalis Per-
gande. These previous results support the possibility our
study that the positive effect of symbiotic association by
AMF on the abundance of the cell-contents feeder Thrips
spp. 18 DAT might be caused by the increased phosphorus
concentration, because of the symbiosis. However, 47
DAT, the abundance of Thrips spp. decreased on plants
treated with mycorrhizal fungi. This result might be
explained by the effect of AMF on induced plant responses
to herbivory (Nishida et al. 2009, 2010), because damaged
plants associated with the AMF G. margarita increased
production of leaf phenolics (defensive compounds), which
have been shown to reduce oviposition by spider mites
(Nishida et al. 2010).
Laboratory studies have shown that AMF negatively
affect the growth and survival of generalist chewers, for
example lepidopteran larvae (Rabin and Pacovsky 1985;
Gange and West 1994; Vicari et al. 2002). For example,
Gange and West (1994) found that AMF increased defen-
sive compound concentrations in foliage, resulting in
reduced growth of the generalist chewer Arctia caja L.
larvae. However, in our study, soybeans with AMF did not
negatively affect the larval abundance of the generalist
chewers, the lepidopteran larvae. Thus, the defensive
compounds which might be induced by AMF may not
affect the abundance of these generalist chewers.
Fig. 2 Therelationship betweenthe abundanceof O. sauteriand Thrips
spp. on soybean plants inoculated with or without Gigaspora margarita
(?M or-M, as representedby closed and open circles, respectively) 18
( y =
exp(-
2.5566 ?
0.021 x)) and 47 ( y =
exp(0.9393 ?
0.0014 x))days after transplanting (DAT)
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The abundance of the predatory bug, Orius spp., is
known to depend on the abundance of prey such as aphids
and thrips (Nagai 1990; Nakata 1995). A previous study
reported that Orius sp. had strong preference for thrips as
their prey (Nagai 1991). For example, Nagai (1991)
showed that Orius sp. preferred melon thrips Thrips palmi
Karny to cotton aphid Aphis gossypii Glover. Similarly, in
our study, numbers of O. sauteri increased in response tothrips abundance but not to aphid abundance. Thus, effects
of AMF on aboveground arthropods might affect the
abundance of predatory bugs by increasing and/or reducing
the abundance of thrips.
Our results partially support the hypothesis that the
effects of AMF on the abundance of foliar-feeding insects
depend on feeding mode (Gange et al. 2002). We also
found that AMF affected the abundance of the predator via
the increased and/or reduced abundance of particular
groups of foliar insects, Thrips spp. Additional studies are
needed to reveal the effect of AMF on the abundance of
aboveground insects in the field, because we do not fullyunderstand the community interactions in a multitrophic
context which result from AMF (van der Putten et al.
2001).
Acknowledgments We thank Dr N. Katayama, Dr T. Takizawa,
and T. Ananto for their valuable comments on the manuscript, and
Professor E.W. Evans for English correction. We also thank three
anonymous reviewers for their valuable suggestions.
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