ARTICLE

Effects of larval densities and the duration since larval infestationon the host-searching behavior of Diadegma semiclausum,a parasitoid of diamondback moth larvae on plants

Yoshitsugu Ohara • Junji Takabayashi

Received: 17 May 2011 / Accepted: 17 January 2012 / Published online: 31 January 2012

� Japan Ethological Society and Springer 2012

Abstract The host-searching behavior of Diadegma

semiclausum, a parasitoid of diamondback moth (DBM)

larvae, was studied in a wind tunnel. Wasps flew prefer-

entially to a cabbage plant, freshly infested by 1 DBM

larva, or one freshly infested by 10 DBM larvae, than to an

intact plant. There was no significant difference between

wasps’ responses to plants infested by different DBM lar-

vae densities. We also found that the duration since the last

infestation by 10 DBM larvae (1 or 3 days) negatively

affected the attractiveness of infested plants. We also

studied the time wasps spent searching for larvae on a

cabbage plant (residence time). The wasps spent ca. 400 s

on a plant freshly infested by 1 larva. Residence time

was significantly longer (ca. 1,200 s) on a plant freshly

infested by either 5 or 15 DBM larvae. Residence time of

D. semiclausum on a plant freshly infested by 5 DBM

larvae was significantly longer than on a previously

infested plant (1 or 3 days after the last infestation). These

results showed that host densities on a plant and the

duration since their last infestation affected the host-

searching behavior of D. semiclausum.

Keywords Diadegma semiclausum � Plutella xylostella �Cabbage plant � Olfactory responses � Residence time

Introduction

Carnivorous natural enemies of herbivorous arthropods are

known to use volatiles produced by herbivore-infested

leaves in their prey finding (e.g., Takabayashi and Dicke

1996; Horiuchi et al. 2003; Sabelis et al. 2007; Arimura

et al. 2009). Studies show that herbivore species and their

developmental stages affect the olfactory response of car-

nivores to prey-infested plant volatiles. Carnivores

responded preferentially to plant volatiles induced by their

prey over those induced by non-prey (e.g., Shiojiri et al.

2000a; De Moraes et al. 1998; Horiuchi et al. 2003). Fur-

thermore, they prefer volatiles from a plant that is infested

by prey of suitable developmental stages (Takabayashi

et al. 1994; Yoneya et al. 2009). Such studies focusing on

the specificity of tritrophic systems are essential for

understanding the ecological significance of tritrophic

interactions.

Once on a prey-infested plant, carnivores start searching

for their prey by using volatile/contact chemicals of either

plant or prey origin, or the combined residue of both left on

prey-infested plants (Sato 1979; Takabayashi et al. 1985;

Takabayashi and Takahashi 1986; Shiojiri et al. 2000b;

Steidle and Fischer 2000; Steidle and Ruther 2000; Maeda

and Takabayashi 2001a; Ohara et al. 2003b; Uefune et al.

2011). Herbivore species also affects the residence time of

prey searching behavior. For example, Sato (1979) reported

that Cotesia glomerata, a parasitoid of cabbage white

butterfly larvae (Pieris rapae), showed characteristic

antennal searching behavior to the open edge of a host-

infested leaf. The search duration was longer than to a non-

host-infested open edge or an artificially damaged edge.

The contact chemicals responsible for this host-specific

response by the wasps are comprised of leaf juice and host

regurgitant (Sato 1979; Horikoshi et al. 1997). Similarly,

Y. Ohara

Mishima High School, Sunto-Gun, Shizuoka 411-0944, Japan

J. Takabayashi (&)

Center for Ecological Research, Kyoto University,

2-509-3 Hirano, Otsu, Shiga 520-2113, Japan

e-mail: Junji@ecology.kyoto-u.ac.jp

123

J Ethol (2012) 30:295–300

DOI 10.1007/s10164-012-0326-0

C. vestalis, a parasitoid of diamondback moth (DBM)

larvae, showed characteristic antennal searching behavior

only to host-infested open leaf edge (Shiojiri et al. 2000b).

It is adaptive for carnivores to find a plant currently

infested by a certain number of prey. Thus, prey density on

a plant (e.g., Maeda and Takabayashi 2001b; Gols et al.

2003; Shiojiri et al. 2010) and duration since the last

infestation (Hanyu et al. 2009; Kugimiya et al. 2010;

Mandour et al. 2011) would be important factors for for-

aging carnivores. We recently reported host-density

dependent/independent response of parasitic wasps to host-

infested plant volatiles (Shiojiri et al. 2010). Cabbage plants

attract more parasitoids (Cotesia glomerata) when there are

more herbivores on the plant (Shiojiri et al. 2010). How-

ever, when cabbage plants are attacked by DBM (Plutella

xylostella) larvae, parasitoids of the larvae (Cotesia ves-

talis) fail to discriminate between herbivore-rich and her-

bivore-poor plants (Shiojiri et al. 2010). Effects of the

duration since the last infestation on the olfactory responses

to infested plants have been reported in tritrophic systems of

corn plants: common armyworms (Mythimna separata) and

parasitic flies Exorista japonica (Hanyu et al. 2009); cab-

bage plants: P. xylostella larvae and C. vestalis (Kugimiya

et al. 2010); and corn plants: common armyworms and

parasitic wasps Cotesia kariyai (Mandour et al. 2011).

Diadegma semiclausum, a solitary parasitoid of

P. xylostella larvae, is thought to be an effective biological

control agent of P. xylostella. In 1993, the wasp was

introduced into Japan from Taiwan to test its effectiveness

(Noda et al. 2000). We previously showed that the wasp

was attracted to herbivore-induced volatiles emitted by

larvae-infested cabbage plants in a wind tunnel (Ohara

et al. 2003a). On the infested plant, the wasp showed

characteristic antennal contact with the host-infested edge

but not with an artificially damaged edge (Ohara et al.

2003a). Both the regurgitant of the host larvae and the juice

of a host plant are essential to elicit the wasp’s antennal

searching on a plant (Ohara et al. 2003a). Effects of host

densities and duration since the last infestations that would

affect foraging behavior of D. semiclausum remain to be

studied. The objectives of this study were to test whether

olfactory response and antennal host-searching behavior of

D. semiclausum is affected by: (1) the number of DBM

larvae on a plant, and (2) the history of infestations.

Materials and methods

Plants and insects

Cabbage plants (Brassica oleracea cv. Shikidori) were

grown separately in 300-ml plastic pots with soil in an

incubator (25 ± 3�C, 60 ± 10% RH, L16:D8) for

approximately 1 month. Plants of ca. 20 cm in height were

used for the experiments.

Eggs of DBM P. xylostella were obtained from the stock

culture of Tohoku National Agricultural Experiment Sta-

tion, and mass-reared on potted plants in a climate-con-

trolled room (25 ± 3�C, 60 ± 10% RH, L16:D8). A

population of D. semiclausum was also obtained from the

stock culture of Tohoku National Agricultural Experiment

Station. Adults of the parasitoid species were fed honey

and contained in a plastic cup (12 cm diameter 9 5 cm

height) in a climate-controlled room (20 ± 2�C, 50–70%

RH, L16:D8) for 2 days to ensure mating. Females were

then kept in a climate-controlled room (15 ± 2�C, 50–70%

RH, L16:D8) until they were tested at 5–12 days old. At

least 1 h prior to each experiment, oviposition-inexper-

ienced females were transferred to another climate-con-

trolled room (25 ± 2�C, 50–70% RH, L16:D8).

Flight response of D. semiclausum to host-infested

plants under different conditions

Experiments were performed in a wind tunnel [50 cm

diameter 9 150 cm length; refer to Ohara et al. (2003a) for

details] in a climate-controlled room (25 ± 2�C, 50–70%

RH). Two potted plants with different treatments were set

20 cm apart at the upwind end of the wind tunnel as odor

sources. For each repetition, a wasp was released down-

wind, from a glass tube (3 cm diameter 9 9 cm length).

We counted the number of wasps that landed on each of the

two treatments (plants). Observations ceased once the wasp

landed on one of the odor sources (treatments). If a wasp

did not land on one of the treatments within 5 min, we

stopped the bioassay. We regarded these wasps as having

made ‘no choice’. We replicated approximately 60 bioas-

says, using different wasp individuals. The experiments

were carried out over 6–7 experimental days. Fresh odor

sources were prepared on each experimental day. Cabbage

plants were inoculated with second and third stadia DBM

larvae, using a fine brush. Similarly, prior to each experi-

ment, DBM larvae were removed from plants with a fine

brush. Damaged leaves were washed with water prior to the

experiments. The following treatments were conducted on

plants for the wind tunnel bioassay:

Treatment (1). An intact cabbage plant.

Treatment (2). A cabbage plant damaged by one larva

for 1 day. We placed a larva on a leaf.

Treatment (3). A cabbage plant damaged by 10 larvae

for 1 day. We placed 2–3 larvae per leaf.

Treatment (4). A cabbage plant damaged according to

treatment (3) was kept in the climate room for 1 day.

Treatment (5). A cabbage plant damaged according to

treatment (3) was kept in the climate room for 3 days.

296 J Ethol (2012) 30:295–300

123

Treatments (1) to (3) were designed to test the flight

response of D. semiclausum to cabbage plants damaged by

different numbers of P. xylostella larvae (Experiment 1).

Plants of treatments (3) to (5) were designed to test the

flight response of D. semiclausum to cabbage plants that

were infested by P. xylostella larvae for different durations

(Experiment 2).

Residence times of D. semiclausum on leaves infested

by larvae at different densities and for different

durations

A potted cabbage plant (ca. 25 cm high) infested by

10 second stadium P. xylostella larvae for 1 day (upwind

odor source) was placed in the wind tunnel, and one cab-

bage leaf (patch: ca. 15 cm high) was placed 50 cm

downwind of the pot. A female wasp was placed in a

capped glass tube (3 cm diameter 9 9 cm length). To

introduce the wasp to a patch, we gently collected it in the

glass tube with an insect aspirator, and allowed it to walk

onto the patch. After release, we measured its residence

time. When the wasp flew away from the patch and landed

on the upwind odor source plant or on the wind tunnel wall,

it was recorded as having left the patch. This experiment

was replicated approximately 20 times, using different

wasps for each experiment. The experiments were con-

ducted over 3–4 days. A fresh odor source was prepared on

each experimental day. Second stadium larvae were care-

fully placed on, and removed from, leaves, using a fine

brush. Prior to the experiments, host larvae were removed.

Leaves were not washed with water for these experiments

because the wash has been shown to reduce the residence

time of wasps (Ohara et al. 2003b). The feces were not

removed either. Plants were treated in the following ways

for the wind tunnel bioassay:

Treatment (1). A cabbage leaf damaged by 1 second

stadium larva for 1 day.

Treatment (2). A cabbage leaf damaged by 5 second

stadium larvae for 1 day.

Treatment (3). A cabbage leaf damaged by 15 second

stadium larvae for 1 day.

Treatment (4). A cabbage leaf damaged according to

treatment (2) was kept in the climate room for 1 day.

Treatment (5). A cabbage leaf damaged according to

treatment (2) was kept in the climate room for 3 days.

Treatments (1) to (3) were to test the effects of the

number of DBM larvae in a patch on the residence time of

D. semiclausum (Experiment 3). Leaves of treatments (2),

(4) and (5) were to test the effect of the duration since the

last infestation of a patch, on the tendency of D. semi-

clausum to leave a patch (Experiment 4).

Statistics

Binomial testing was used for Experiment 1 and 2. Scheffe

post hoc test was used for Experiment 3 and 4.

Results

Experiment 1: flight responses of D. semiclausum

to cabbage plants damaged by different P. xylostella

larval densities

Diadegma semiclausum showed a significant preference for

plants damaged by either 1 or 10 larvae over the undam-

aged plant (Fig. 1; binomial test, P \ 0.0001). However,

wasps were equally distributed between the plants infested

by 1 larva versus those infested by 10 larvae (Fig. 1;

binomial test, P = 0.36).

Experiment 2: flight responses of D. semiclausum

to cabbage plants of different durations since the last

infestation by P. xylostella larvae

Wasps preferred the newly damaged plant to the damaged

plant 1 day after the last infestation (Fig. 2). The damaged

plant 1 day after the last infestation was favored over the

damaged plant 3 days after the last infestation (Fig. 2:

binomial test, P \ 0.01).

Experiment 3: effect of DBM larvae density

on patch-leaving decision by D. semiclausum

Wasps stopped at a host-damaged leaf edge and made

obvious antennal contact with the edge. The wasps spent a

significantly shorter residence time on a patch damaged by

NCPlants damaged by 10 larvae

Intact plants

Plants damaged by one larva

NC

19***

Intact plants

Plants damaged by 10 larvae Plants damaged by one larva

16

***

40 20 0 20

18NS

The number of D. semiclausum

Fig. 1 Response of D. semiclausum in a wind tunnel to cabbage

plants infested by host larvae versus intact cabbage plants.

***P [ 0.001; NS not significantly different (binominal test)

J Ethol (2012) 30:295–300 297

123

1 larva than on a patch damaged by 5 or 15 larvae (Fig. 3:

one-way ANOVA, F2,58 = 15.268, P \ 0.0001; Scheffe’s

test, P \ 0.0001). Consequently, it appears that these

wasps can evaluate the density of host larvae on a patch

and adapt their residence time accordingly.

Experiment 4: Effects of the duration since the last

infestation in a patch on residence time

of D. semiclausum

The wasps had a significantly longer residence time on a

newly damaged patch than on a damaged patch either 1 or

3 days after the last infestation (Fig. 4: one-way ANOVA,

F2,61 = 10.116, P \ 0.0002; Scheffe’s test, P \ 0.005).

Residence times were not significantly different between

damaged patches tested 1 versus 3 days after infestation

(Fig. 4: Scheffe’s test, P = 0.869).

Discussion

Diadegma semiclausum responded equally to volatiles of

cabbage plants infested by 1 DBM larva and those of cab-

bage plants infested by 10 DBM larvae. The range of DBM

abundances per plant roughly resembled that observed on

cabbage plants in the field, as well as on some related wild

plants in Japan, like Rorippa indica and Brassica juncea

(J. Abe and M. Uefune, personal observation). This suggests

that foraging D. semiclausum use volatiles produced by

DBM-infested cabbage plant in the field to locate their

hosts. Since we did not measure the area damaged by DBM

larvae, we could only infer (from Shiojiri et al. 2010), that

areas damaged by 1 versus 10 DBM larvae, are less than 2%

and ca. 10% of a plant, respectively. It remains to be

answered whether cabbage plants that sustain less than

2–10% damage, produce sufficient volatiles consistently

enough to attract D. semiclausum.

The wasps can evaluate the duration since the last

infestation by detecting changes in attractants produced by

infested plant (Experiment 2). This would help the wasps to

find newly infested plants by distinguishing between pre-

viously and currently infested plants in the field. Similar

results have been reported in tritrophic systems (Hanyu

et al. 2009; Kugimiya et al. 2010; Mandour et al. 2011).

For example, in a tritrophic system of corn plants, Mythi-

mna separata larvae, and the parasitic wasp Cotesia kar-

iyai, the attractiveness of the infested plants to C. kariyai

was significantly higher than that of intact plants when the

time since the last infestation was within 1 day (Mandour

et al. 2011).

Newly damaged plantsDamaged plants 1 dayafter the last infestation

NC

Damaged plants 1 dayafter the last infestation

Damaged plants 3 daysafter the last infestation

18

***

18**40 20 0 20

The number of D. semiclausum

Fig. 2 Response of D. semiclausum in a wind tunnel to cabbage

plants with different durations since the last infestation by P. xylostellalarvae. ***P [ 0.001; **0.01 [ P [ 0.001 (binominal test)

1200

1600

Resident time (sec)

bb

400

800

1200

a

01 5 15

Number of larvae on a patch

Fig. 3 Residence time of D. semiclausum (seconds, mean and

standard error) in a patch infested by different numbers of host larvae

in a wind tunnel. Bars with the same letters are not significantly

different (P \ 0.05), using Scheffe’s test

Resident time (sec)

800

1200

b

a

b

0

400

0 1 3

Number of days after the last infestation

Fig. 4 Effects of the duration since the last infestation in a patch on

the residence time of D. semiclausum (seconds, mean and standard

error) in a wind tunnel. Bars with the same letters are not significantly

different (P \ 0.05), using Scheffe’s test

298 J Ethol (2012) 30:295–300

123

We have already reported that D. semiclausum uses

multiple cues (such as host feces, silks, and chemicals left

on the leaf surface by the host larvae) in the current patch

for their patch-leaving decision (Ohara et al. 2003b). The

response of the wasps to such complex cues reached a

plateau at 5 larvae per patch (Experiment 3). Thus, the

appeal of a 5 larvae-damaged patch and a 15 larvae-dam-

aged patch were roughly equivalent for the wasps. As

mentioned above, the abundances per plant roughly match

that observed in the field. Similar results were reported by

Maeda et al. (1998): the residence time of the predators in

patches with 40 eggs and those with 140 eggs did not differ

significantly.

It would clearly be adaptive for the wasps to stay a

shorter length of time in a patch where the host larvae had

departed more than 1 day previously than in a newly

infested patch (Experiment 4). The wasps’ residence times

did not differ significantly between patches of 1 versus

3 days after infestation. So it is suggested that the chemical

cues on leaf surfaces that wasps use to evaluate the dura-

tion since infestation in a patch probably decrease critically

within a day.

To use carnivores for pest management, it is important

to know whether, and if so how, carnivores use volatile/

contact infochemicals from plants, herbivores, and/or

plant–herbivore complex origins. In this study, we showed

that biotic factors such as host densities on a plant and the

duration since the last infestation affected the host-

searching behavior of D. semiclausum. Further, abiotic

factors would also affect carnivores’ responses (e.g.,

Takabayashi et al. 1994; Maeda et al. 2000). These factors

should also be studied for the effective use of D. semi-

clausum as a pest management agent.

Acknowledgments This research was partly supported by a Grant-

in-Aid for Scientific Research (S) (No. 19101009), JSPS Core-to-Core

project, and by the Global Center of Excellence Program ‘‘Formation

of a Strategic Base for Biodiversity and Evolutionary Research: from

Genome to Ecosystem’’ of Kyoto University.

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