3. efecto de hma sobre la abundancia de insectos foliares ueda2013

8/18/2019 3. Efecto de HMA Sobre La Abundancia de Insectos Foliares Ueda2013

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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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Appl Entomol Zool (2013) 48:79–85

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.

80 Appl Entomol Zool (2013) 48:79–85

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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

Appl Entomol Zool (2013) 48:79–85 81

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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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3. efecto de hma sobre la abundancia de insectos foliares ueda2013

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