Ecological and morphological characteristics of the endoparasitoids of larval Acronicta rumicis...

Entomological Research

36

(2006) 208–215

© 2006 The AuthorsJournal compilation © 2006 The Entomological Society of Korea and Blackwell Publishing Asia Pty Ltd

Blackwell Publishing Ltd

RESEARCH PAPER

Ecological and morphological characteristics of the endoparasitoids of larval

Acronicta rumicis

(Lepidoptera: Noctuidae)

Youngho CHO

1,†

, Ohseok KWON

2,†

and Sang-Ho NAM

1

1 Department of Biology, Daejeon University, Daejeon, Korea 2 National Institute of Agricultural Science and Technology, RDA, Suwon, Korea

Correspondence

Sang-Ho Nam, Department of Biology, Daejeon University, Daejeon 300-716, Korea. Email: [email protected]

†

These authors contributed equally to this paper.

Received 30 July 2006; accepted 28 August 2006.

doi: 10.1111/j.1748-5967.2006.00035.x

Abstract

The Hymenopterans

Glyptapanteles liparidis

,

Microplitis

sp. and

Diadegma

sp. were found to be larval parasitoids and koinobionts of

Acronicta rumicis

(Lepidoptera: Noctuidae).

Mesochorus semirufus

is believed to be a new unreportedhyperparasitoid of

G. liparidis

, which, along with

M. semirufus

, is a gregariousparasitoid. In contrast, the parasitoids

Microplitis

sp. and

Diadegma

sp. are solitary.All of the hymenopteran parasitoids are multivoltine insects that emerge from

A. rumicis

more than once

. Compcilura concinnata

,

Euexorista

sp. and

Exorista

sp. of the Diptera were found to be larval–pupal parasitoids, solitary parasitoidsand koinobionts. These three species are univoltine, and emerge only once from

A. rumicis.

Morphological and life cycle data were collected for

G. liparidis

, andfor the parasitoids of that species found in this study. The major and minor axes ofan egg of

G. liparidis

were 0.10 and 0.02 mm, respectively, while the mean clutchsize of

G. liparidis

was 67.71

±

39.36 individuals. The body length of femaleand male

G. liparidis

were 2.25

±

0.06 and 2.21

±

0.12 mm, respectively, and thelongevity of an adult was 2.93

±

0.96 days. Among the parasitoids, the mean bodylength of an adult

Microplitis

sp. was 3.5 mm and adults lived for an average of8.13

±

3.54 days. The adult

Diadegma

sp. was larger (mean body length 6.5 mm)but lived for a shorter interval (3.33

±

1.32 days). The body lengths of female andmale

M. semirufus

were 3.16

±

0.11 and 3.10

±

0.23 mm, respectively, greater thanthe body lengths of female and male

G. liparidis

. The body lengths of adult

C. concinnata

,

Euexorista

sp. and

Exorista

sp. were 9.5, 9.53 and 8.68 mm,respectively. All of their pupae were dark brown.

Key words:

Acronicta rumicis

, Braconidae, Ichneumonidae, Tachinidae, parasitoid.

Introduction

Parasitoids can be found in the Hymenoptera, Diptera,Coleoptera, Lepidoptera and Neuroptera. There are 50 000species of hymenopteran parasitoids, 15 000 species ofdipteran parasitoids and 3000 species of other parasitoids(Eggleton & Belshaw 1992). Taken together, parasitoidsmake up 8.5% of all insects (Gaston 1991). Eighty percent ofparasitoids are parasitic wasps (Quicke 1997), which aredivided into two groups: Symphyta and Apocrita. Membersof the Symphyta are phytophagous, and only 75 species have

been reported worldwide. Among the Apocrita, the Ichneu-monidae is the largest family, with 15 000 described speciesand the second largest family is the Braconidae, with 10 000species. The third largest taxon of parasitoids is the dipteranfamily Tachinidae, with 8000 species (Godfray 1994).

Even in northern Europe where the fauna is well studied,it is still difficult to identify members of some genera andsubfamilies of Hymenoptera at the species level (Godfray1994). For this reason, many entomologists believe that thereare many more parasitoids than have been recorded so far.Gaston (1991) estimates that there may be approximately

Characteristics of endoparasitoids on

A. rumicis


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8 million species of insects in the world. Godfray (1994) esti-mates that parasitoids worldwide make up approximately20–25% of all insects; thus there is perhaps a total of 1.6 to2 million species.

Parasitoids have a relatively high diversity compared toother insect groups. As they have unique life histories, theyoften become the targets of ecological studies. They aresometimes used as important agents of biological control,which requires a thorough understanding of their impactson economic species (Debach 1974; Mills & Getz 1996;Murdoch & Briggs 1996). Despite the numerous species ofparasitoids, and the many individuals that have been used tocontrol other insect groups (thus showing their critical role inthe ecosystem), only a small amount of research has beendone on parasitoids in Korea.

The present study deals with parasitoids of

Acronicta rumicis

larvae that live on

Rumex obtusifolius

, a naturalized plant.Although

A. rumicis

larvae also live on the fruit trees

Persi-caria

spp.,

Prunus

spp. and Polygonaceae (Kim

et al

. 1982;Lee & Chung 1997; Mutuura

et al

. 1975), Cho (2000) foundthat the

A. rumicis

larvae complete their life cycles success-fully on

R. obtusifolius

. In a previous study of the parasitesof larval

A. rumicis

, two orders, three families and eightspecies of endoparasitoids were reported (Cho 2004). Theimmediate purpose of this work was to show the ecologicaland morphological characteristics of the endoparasitoidsof

A. rumicis

larvae that have adequately adapted to

R. obtusifolius

, and ultimately to understand the mutualinteraction between the plants, herbivores and parasitoids.

Materials and methods

Acronicta rumicis

larvae were collected during a period from2000 to 2002 from several regions within the city of Daejeon,Korea: Yongun-dong, Panam-dong and Secheon-dong ofDong-gu. Collections were carried out at the investigationsites two to three times a month between May and October,the interval during which the larvae appeared. Larvae werecollected while they were feeding on host plants in fallowfields, streams and valleys that were drier than most places.

Each

A. rumicis

larva was collected in the field and wasreared separately in the laboratory. In the growth chambers,daytime conditions were maintained at 25

°

C, 75% relativehumidity (RH) and 12 000

±

100 lx. At night, the temperatureand RH were kept the same, but light was 0 lx. The photo-period was 14 h light : 10 h dark (LD 14:10). Filter paper(85 mm; Whatman no. 2; Whatman, Maidstone, Kent, England)was put on a Petri dish (100 mm diameter

×

15 mm height)in which each

A. rumicis

larva was reared. The filter paperwas replaced daily. Humidity was maintained by regularlyadding 1 mL distilled water. Any waste inside the Petri dishwas washed out with 70% alcohol every day, after which thedish was dried. The conditions under which the parasitoids

were raised were the same as those for the host insects. Ifemergence of parasitoids was found, 10% sucrose solutionwas supplied daily by wetting it on cotton.

The collected

A. rumicis

larvae were raised on leaves of

R. obtusifolius

undamaged by other insects or viruses. Theleaves were washed in flowing water to remove dust andforeign substances and then the water was removed. Using asharp round tool of 1017.36 mm

2

with costa in the center,leaves of

R. obtusifolius

were regularly cut and provided tothe larvae. When parasitoids escaped from it emerged from alarva, a piece of leaf was supplied to see if the

A. rumicis

larva tried to eat it or not. When

A. rumicis

larvae entered theprepupa stage, they stopped feeding on the leaves.

A stereo microscope (SMZ-2T; Nikon, Tokyo, Japan) andimage analysis system (BMI, version 4.0; BumMi Universe,Seoul, Korea) was used to measure the body, antenna, forewinglength, head capsule width, cocoons and pupae of the driedmale and female parasitoids that emerged from

A. rumicis

larvae. Only the parasitoids of particular interest, such as

G. liparidis

,

Microplitis

sp. and

M. semirufus

were measuredin detail. Only the general dimensions of the other parasitoidswere measured. The body size of both male and femaleparasitoids was measured from their heads to the ends of theirabdomens down the centerline, along the side of their bodies.Antennae and wings were measured after flattening them. Thewidth of the head capsules was measured after removingeach head and placing it on a flat surface. Next, the distancebetween compound eyes, on the anterior plane, was measured.Finally, the major and minor axes of each cocoon and pupawere measured.

Hyperparasitism occurred in some individuals of both

G. liparidis

and

M. semirufus

. Body sizes were determinedfor 20 females and 20 males of

G. liparidis

and for 10 femalesand 8 males of

M. semirufus.

For comparison of body sizes,30 females and 30 males of

G. liparidis

were randomlyselected from cocoons that did not have hyperparasitism, andwere measured.

The group sizes were small, so a nonparametric test(Mann–Whitney

U

-test) was used for the statistical analysis.This was carried out using

spss

(version 10.0; SPSS, Chicago,IL, USA).

Results and discussion

Ecological characteristics of parasitoids

As reported by Kim (1970), and by Yasumatsu and Watanabe(1964),

G. liparidis

is a larval parasitoid of

A. rumicis.

It hasbeen shown that the larva of

A. rumicis

still molts and eatsafter being parasitized, so

G. liparidis

is considered to bea koinobiont. Hoch and Schopf (2001), Marktl

et al

. (2002)and Watanabe (1942) reported that

G. liparidis

is a gregariousparasitoid (because many

G. liparidis

individuals emerge

Y. Cho

et al.

210


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from just one larva of

A. rumicis

), and Kenis and Vaamonde(1998) reported that it is a multivoltine insect that generatesseveral times a year. Our results suggested that it is amultivoltine insect because it appeared from May to October,except during June (Table 1).

The wasps

Microplitis

sp. (Braconidae) and

Diadegma

sp.(Ichneumonidae) are also parasitoids of larval

A. rumicis

.Both are also koinobionts because

A. rumicis

larvae molt andeat as usual after being parasitized by them. However, theyare different to multivoltine parasitoids of

G. liparidis

: asingle wasp completes its life cycle using only one individuallarva of

A. rumicis

(Table 1). There are 21 reported species of

Microplitis

in Korea, and they are known as endoparasitoidsof Lepidoptera.

Microplitis heterocera

is parasitic on

Acronictapsi

, a species similar to

A. rumicis

, and

M. mediana

is knownto be a polyphagous parasitoid with more than 30 host species(Yeo & Park 1998).

Diadegma

sp. is an unrecorded genus inKorea that is widely used as an insect enemy of

Plutellaxylostella

, an important pest for

Brassica campestris

subsp.

napus

var.

pekinensis

,

Raphanus sativus

var.

hortensis

for.

acanthiformis

and Cruciferae (Idris & Grafius 1993; Talekar& Yang 1993; Yang

et al

. 1993). In Indonesia, successful

control of P. xylostella was reported after the normal rate ofparasitism was increased by 96% by using D. eucerephaga(Waterhouse & Norris 1987).

The members of the Mesochorinae are known as hyper-parasitoids, and according to reports there are approximately10 species in Korea (Lee & Cha 2000; Cha et al. 2001).M. semirufus is a hyperparasitoid (Hochberg & Ives 2000)previously unrecorded in Korea, and it appeared during thecourse of our study (Table 1; Cho et al. 2006). In the presentstudy, it was also found to be a hyperparasitoid of G. liparidisfor the first time. It is clearly a gregarious parasitoid becausemany individuals emerged together from the same host, andit is a bivoltine or multivoltine insect because it appeared inMay and October.

Compcilura concinnata, Euexorista sp. and Exorista sp.(Tachinidae) are larval–pupal parasitoids. They emerged duringthe prepupa stage after parasitizing the larvae of A. rumicis.Larvae of A. rumicis could molt even when parasitized byC. concinnata, Euexorista sp. or Exorista sp, indicating thatall these three Tachinidae are koinobionts. All three speciesare solitary, because each one emerges from one individualA. rumicis larva. They are also univoltine, appearing only

Month Gly Mic Ich Dia Tac Com Eue Exo G+M G+T G+C M+C

2000

May 4 0 1 4 1 0 0 0 2 0 0 0June 0 0 1 3 0 0 2 0 0 0 0 0July 2 0 0 2 0 0 0 0 0 0 0 0August 1 1 0 1 0 0 0 0 0 0 0 0September 1 0 0 1 0 0 0 0 0 0 0 0October 4 8 0 0 2 1 0 1 0 1 1 1Total 12 9 2 11 3 1 2 1 2 1 1 0

2001


2002


Gly, Glyptapanteles liparidis; Mic, Microplitis sp.; Ich, Ichneumonidae; Dia, Diadegma sp.; Tac, Tachinidae; Com, Compcilura concinnata; Eue, Euexorista sp.; Exo, Exorista sp.; G+M, G. liparidis and Mesochorus semirufus (hyperparasitism); G+T, G. liparidis and Tachinidae (multiparasitism); G+C, G. liparidis and C. concinnata (multiparasitism); M+C, Microplitis sp. and C. concinnata (multiparasitism).

Table 1 Monthly species composition ofendoparasitoids on Acronicta rumicis larvae(2000–2002)

Characteristics of endoparasitoids on A. rumicis

Entomological Research 36 (2006) 208–215 211© 2006 The Authors. Journal compilation © 2006 The Entomological Society of Korea and Blackwell Publishing Asia Pty Ltd

once a year (Tables 1, 2). For C. concinnata, the results fromour work did not match the results from some earlier studies.Ichiki and Shima (2003), Kenis and Vaamonde (1998), andPemberton et al. (1993) reported C. concinnata to be a multi-voltine insect appearing at least twice a year and a gregari-ous parasitoid in that several individuals occurred in theparasitized host. C. concinnata has 161 reported host speciesin North America (Arnaud 1978) and 59 host species in Japan(Shima 1999). Also, the host specificity of parasitic flies isgenerally lower than that of parasitic wasps (Debach 1974).C. concinnata is a polyphagous insect parasitoid needing analternate host (Kenis & Vaamonde 1998) and it prefers aqualified host as food for the next generation because of itsparasitoid nature (Quicke 1997). Thus, when the quality ofthe hosts is not good, it maintains a solitary life (Godfray1994) by restricting its clutch size (Heimpel & Rosenheim1998). It can also use other hosts that offer good nutritionalconditions as food. Therefore, it is reasonable thatC. concinnata was classified as a polyphagous and gregariousparasitoid by Kenis and Vaamonde (1998).

Morphological characteristics and life cycles of

parasitoids

Glyptapanteles liparidisThe lengths of the major and minor axes of a G. liparidis eggwere 0.10 and 0.02 mm, respectively, and the shape wasoblong (Fig. 1). The surface of the egg was very smooth.When I observed an egg using a phase-contrast microscope2 days after the death of its mother, the egg was alive. Theeggs of Braconidae have a short tail, so they are differentfrom those of the Pteromalidae, which have no tail, and fromthe Cynipidae, which have a long tail. Also, the eggs of theIchneumonidae have tails on both sides, so they are totally

different from the eggs of the Braconidae (Hinton 1981; Rosset al. 1982).

The mean clutch size of G. liparidis was 67.71 ± 39.36individuals. Its development from cocoon to adult took7.94 ± 2.33 days, and the longevity of an adult was 2.93 ±0.96 days. The color of the cocoon was yellow, the length ofthe major axis was 17.44 ± 1.63 mm, the length of the minoraxis was 14.37 ± 1.17 mm, and the height was 9.63 ± 1.24 mm.After a G. liparidis emerged from a larva of A. rumicis, thelarva survived for 2.14 ± 0.69 days, but did not feed (Table 3).Watanabe (1942) reported that 20 G. liparidis individualsemerged from one host. This is less than the mean clutch sizeof 67.71 ± 39.36 individuals observed in the present study.

Measurements of female and male G. liparidis: bodylength, 2.25 ± 0.06 and 2.21 ± 0.12 mm; length of antenna,2.50 ± 0.12 and 2.60 ± 0.06 mm; length of forewing, 2.35 ±0.08 and 2.25 ± 0.05 mm; and width of head capsule,0.61 ± 0.02 and 0.59 ± 0.01 mm, respectively (Figs 2, 9).There was no difference in body length between the sexes.The male’s antennae were bigger than the female’s, and thefemale’s head capsule width and forewing length weregreater than the male’s (Fig. 9). Kim (1970) reported that thebody lengths of female and male G. liparidis were 3.2 ± 3.8and 2.8 ± 3.2 mm, and the widths of the head capsule were3.4 ± 4.0 and 3.2 ± 3.6 mm, respectively. The length of thebody as measured by Kim (1970) was 1 mm longer than ourresult. The difference in the two observations could arisefrom the difference in measuring a live or a dead individual.It appears that there is a big difference between thepresent study and Kim’s report. However, Ku et al. (2001)reported body lengths of 2.5 ± 3.5 mm (with no differencebetween the sexes), and Yasumatsu et al. (1976) reportedbody lengths of 3 mm; both are similar to the results of ourpresent work.

Table 2 Ecological characteristics of endoparasitoids of Acronicta rumicis larvae

Parasitized host stage

Parasitoid escape stage

Parasitized host ecdysis

Food consumptionof parasitized host

Solitary (S) or gregarious (G)

Idiobiont (I) orkoinobiont (K)

Univoltine (U) ormultivoltine (M)

Hymenoptera

Braconidae

Glyptapanteles liparidis Larva Larva Yes Yes G K MMicroplitis sp. Larva Larva Yes Yes S K MIchneumonidae

Diadegma sp. Larva Larva Yes Yes S K MMesochorus semirufus ? ? ? ? G K M

Diptera

Tachinidae

Compcilura concinnata Larva Pupa Yes Yes S K UEuexorista sp. Larva Pupa Yes Yes S K UExorista sp. Larva Pupa Yes Yes S K U

Y. Cho et al.

212 Entomological Research 36 (2006) 208–215 © 2006 The Authors. Journal compilation © 2006 The Entomological Society of Korea and Blackwell Publishing Asia Pty Ltd

Microplitis sp.The mean body length of Microplitis sp. was 3.5 mm andthe forewing length was approximately 3.32 mm (Fig. 3). Themean body lengths and forewing lengths of five species of thegenus Microplitis (M. albotibialis, M. heterocera, M. mediana,M. scrophulariae and M. tadzhica) in Korea, reported byYeo and Park (1998) were 3.23:2.95, 2.7:2.15, 3.38:2.85,

2.79:2.54 and 3.1:2.9 mm, respectively; these are smallermeasurements than those found in our present study.Microplitis sp. emerged as an adult 10.29 ± 3.64 days aftercocoon formation, and the longevity of an adult was8.13 ± 3.54 days. The dimensions of the cocoon in terms ofmajor and minor axes were 4.34 ± 0.66 and 2.02 ± 0.27 mm,respectively (Table 3). The cocoon is usually attached to the

Figures 1–8 Endoparasitoids of Acronicta rumicis larvae. 1 Glyptapanteles liparidis (egg); 2 G. liparidis (female); 3 Microplitis sp. (male);4 Diadegma sp. (male); 5 Mesochorus semirufus (female); 6 Compcilura concinnata (female); 7 Euexorista sp. (female); and 8 Exorista sp.(female). Scale bars, 0.02 mm (1); 1 mm (2–8).



end of the A. rumicis abdomen and it prevents the A. rumicislarva from moving. The A. rumicis larva survived an averageof 10.31 ± 2.63 days after Microplitis sp. escapes, and it doesnot feed during this time.

Diadegma sp.The mean body length of Diadegma sp. was approximately6.5 mm, and the body color was dark on the whole althoughthe color of the legs was yellow (Fig. 4). It took 7.75 ±1.22 days for an adult to emerge from its own cocoon afterescaping from the larva of A. rumicis. The adult longevity ofDiadegma sp. was 3.33 ± 1.32 days, and the lengths of themajor and minor axes of the cocoon were 6.55 ± 0.58 and2.28 ± 0.15 mm, respectively (Table 3). The cocoon has twostripes of white and gray. The larva of A. rumicis doesn’t feedafter the escape of Diadegma sp. because it dies soon after.

Mesochorus semirufusMeasurements for female and male M. semirufus were: bodylength, 3.16 ± 0.11 and 3.10 ± 0.23 mm, length of antenna,

4.00 ± 0.17 and 4.23 ± 0.16 mm; length of forewing, 2.76 ± 0.06and 2.57 ± 0.16 mm; and head capsule width, 0.76 ± 0.03 and0.74 ± 0.03 mm, respectively (Figs 5, 10). The male’s antennaewere longer than the female’s, but there was little difference inthe body length and the head capsule width between sexes. Inboth sexes, the antennae are longest, next is body length andthen forewing length. Morley (1915) reported the body length ofM. semirufus as 8 mm. This is suspicious because there is sucha big difference compared to the results from our present work.

Hyperparasitism was observed for G. liparidis andM. semirufus four times from 2000 to October 2002 (Table 1).The female’s body length of G. liparidis and M. semirufus inwhich hyperparasitism appeared was 2.25 ± 0.08 and 3.10 ±0.11 mm, respectively, and the male’s was 2.22 ± 0.12 and3.10 ± 0.23 mm (Fig. 11). This means that the body length ofM. semirufus was longer than that of G. liparidis in bothsexes. In the present study, we found that the body length ofG. liparidis in both sexes was approximately 1 mm smallerthan, or around one-third of, M. semirufus. Generally, if ahost is smaller than its parasitoid, the possibility of a

Table 3 Ecological characteristics of Glyptapanteles liparidis, Microplitis sp. and Diadegma sp.

No. parasitoidsper host

Time of cocoon to

adult (days)

Longevity of parasitoids in

adult stage (days) Size of cocoon (mm)

Longevity of Acronicta rumicis larva after escape parasitoid (days)

Food consumption of Acronicta rumicis larvaafter escape parasitoid

G. liparidis 67.71 ± 39.36 7.94 ± 2.33 2.93 ± 0.96 17.44 ± 1.63 (major axis) 2.14 ± 0.69 No14.37 ± 1.17 (minor axis)9.63 ± 1.24 (height)

Microplitis sp. 1 10.29 ± 3.64 8.13 ± 3.54 4.34 ± 0.66 (major axis) 10.31 ± 2.63 No2.02 ± 0.27 (minor axis)

Diadegma sp. 1 7.75 ± 1.22 3.33 ± 1.32 6.55 ± 0.58 (major axis) 0 No2.28 ± 0.15 (minor axis)

Figure 9 Morphological characteristics of Glyptapanteles liparidis.�, Female; �, male.

Figure 10 Morphological characteristics of Mesochorus semirufus.�, Female; �, male.

Y. Cho et al.

214 Entomological Research 36 (2006) 208–215 © 2006 The Authors. Journal compilation © 2006 The Entomological Society of Korea and Blackwell Publishing Asia Pty Ltd

deformed parasitoid is high (Godfray 1994), and it will bedifficult for it to complete its life history. That is, it is difficultto judge whether M. semirufus individuals will completetheir life histories after ovipositing on a larva or an egg of anindividual G. liparidis. Thus, it is likely that a larva ofM. semirufus completely consumes one larval G. liparidisinside the A. rumicis larval host after which it escapes andagain cannibalizes another individual. However, becauseresearch about the biology of hyperparasitoids is lacking(Hochberg & Ives 2000) and because the focus of this workwas different, it is not possible to provide firm conclusionsuntil more study is conducted in the future.

Compcilura concinnata, Euexorista sp., Exorista sp.The body length of the C. concinnata female was approxi-mately 9.5 mm (Fig. 6). This figure is similar to the length of8 to 10 mm reported by Yasumatsu et al. (1976). The pupa’scolor was dark brown, the length of its major axis was7.3 mm and its minor axis 3.7 mm. It takes approximately2 weeks for an adult to emerge after becoming a pupa, and itssurvival period is approximately 1 week. Euexorista sp. andExorista sp. are previously unrecorded genera in Korea, andthey appeared as pupa in an A. rumicis prepupa in June 2000and in October 2000, respectively (Table 1). The color of thepupa of both Euexorista sp. and Exorista sp. was dark brownand the body length of an adult female was 9.53 and8.68 mm, respectively (Figs 7, 8).

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Ecological and morphological characteristics of the endoparasitoids of larval Acronicta rumicis...

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