Entomological Research

37

(2007) 103–107

© 2007 The AuthorsJournal compilation © 2007 The Entomological Society of Korea and Blackwell Publishing Asia Pty Ltd

Blackwell Publishing Ltd

RESEARCH PAPER

Effect of host age on life cycle and morphological characteristics of

Glyptapanteles liparidis

(Hymenoptera: Braconidae), a parasitoid of

Acronicta rumicis

(Lepidoptera: Noctuidae)

Youngho CHO

1

, Ohseok KWON

2

and Sang-Ho NAM

1

1 Department of Biology, Daejeon University, Daejeon, Korea2 Division of Applied Biology and Chemistry, School of Applied Biosciences, Kyungpook National University, Daegu, Korea

Correspondence

Sang-Ho Nam, Department of Biology, Daejeon University, Daejeon 300-716, Korea. Email: shnam@dju.ac.kr

Received 29 January 2007; accepted 15 March 2007.

doi: 10.1111/j.1748-5967.2007.00061.x

Abstract

The life cycle of

Glyptapanteles liparidis

was 23.75

±

1.26, 21.95

±

2.44 and20.83

±

0.78 days when fed on the first, second and third instar larvae of

Acronictarumicis

, respectively. Although insufficient numbers hindered statistical analysis,the life cycle of

G. liparidis

appeared to be shortest, 19 days, when fed on fourthinstar larvae. The life cycle of

G. liparidis

tends to shorten as the larvae of

A. rumicis

fed upon are more advanced. The body length, forewing length and headcapsule width of female

G. liparidis

fed on first instar larvae of

A. rumicis

weregreater than those of males, while the antennae of males were longer than those offemales. When fed on second instar larvae, there was no difference in body lengthand head capsule width between males and females, but the male antennae werelonger than the female, and the female forewings were longer than the male. Whenfed on third instar larvae, there was no significant difference in head capsule widthbetween the sexes, but female body length and forewing length were greater thanthe male, and the male antennae were longer than the female. On the whole, femaleswere bigger than males in terms of body length and forewing length, while antennaeof the males were longer than those of the females. There was no difference in headcapsule width between males and females. Body length, antenna length, forewinglength and head capsule width of male and female

G. liparidis

were relatively largerwhen fed on first instar larvae of

A. rumicis

than when fed on second and thirdinstar larvae.

Key words:

Acronicta rumicis

,

Glyptapanteles liparidis

, host–parasitoid interaction, host age.

Introduction

Acronicta rumicis

(Lepidoptera: Noctuidae: Acronictinae)appears biannually throughout the Korean peninsula and theEurasian Region (Kim

et al

. 1982; Shin 2001). The larvaeappear in June as well as in the period August to September,and the emergence of pupae takes place in November (Lee &Chung 1997). The larvae eat leaves of fruit trees, such as

Maluspumila

var

. dulcissima

and

Pyrus

spp., or leaves of treescommonly occurring in the city, such as

Prunus

spp. and

Populus

spp.

A. rumicis

are polyphagous insects that eat

Persicaria

spp.and

Rumex

spp. in the Polygonaceae (Cho 2000; Kim

et al

.1982; Mutuura

et al

. 1975). They may hinder the growth ofyoung trees, as they prefer their new leaves (Lee & Chung 1997).

Individuals belonging to

Glyptapanteles liparidis

(Hymenop-tera: Braconidae) are widely found throughout the Koreanpeninsula and the Eurasian Region (Kim 1970; Ku

et al

.2001). The host insects of

G. liparidis

are

Dendrolimusspectabilis

,

Hyphantria cunea

and

Lymantria dispar

, whichare known to harm the forest ecosystem (Kim 1967; Kim

Y. Cho

et al.

104

Entomological Research

37

(2007) 103–107 © 2007 The Authors. Journal compilation © 2007 The Entomological Society of Korea and Blackwell Publishing Asia Pty Ltd

1970; Ku

et al

. 2001; Yasumatsu & Watanabe 1964). Parti-cularly in Europe,

G. liparidis

are known to exist in largestnumbers amongst the braconids that live upon

L. dispar

,notoriously harmful insects for oak trees (Fuester

et al

. 1983).

G. liparidis

were the first to be introduced to prevent thespread of

L. dispar

in the US in 1909 (Burgess & Crossman1929). In Korea, they are mostly known as an endoparasitoidon

A. rumicis

(Cho 2004; Cho

et al

. 2006).Studies on host–parasitoid interaction provide useful

information for biological control (Godfray 1994; Hassell2000; Hochberg & Ives 2000). In general, if the host insectsare very small compared to the parasitoids, the probability ofdeformation of the latter is high (Godfray 1994). However,most parasitoids tend to lay more eggs in bigger hosts. Stud-ies on optimal parasitism should take the sex ratio, fecundity,life cycle of parasitoids, morphological size and other factorsinto consideration (Godfray 1994; Hardy

et al

. 1992; Harvey2000; Vet

et al

. 1993; West

et al

. 2001; Zaviezo & Mills 2000).Because

G. liparidis

adults survive for only two days,according to Cho (2004), it is essential to relate optimal para-sitism of the parasitoid to the age of the host in order to use

G. liparidis

as a biological control agent against

A. rumicis

.The objective of the present study was to collect biologicaldata with which to reduce or prevent

A. rumicis

from harm-ing forest and city trees, and to examine the effects of age ofthe

A. rumicis

host larvae on the life cycle and morphologyof

G. liparidis

.

Materials and methods

Fifty

A. rumicis

larvae were collected in Yongun-dong,Dong-gu, Daejeon, Korea, in June and July, 2003. Thirty-twoof these non-parasitized larvae emerged to adult form andwere induced to oviposition after mating. The first throughfourth instar larvae that hatched during the same period wereused as hosts for

G. liparidis

.

G. liparidis

cocoons wereformed in 12 out of 18 parasitized hosts.

G. liparidis

thatreared the first generation were used for the experiment.Thirty healthy larvae were picked from the groups of first tofourth instars of

A. rumicis

and put into a plastic container(8 cm wide

×

13 cm long

×

5 cm high) along with 10 femalesand two males of

G. liparidis

that had emerged within 1 hpreviously. Each of them was parasitized by introduction to

G. liparidis

for 5 h.The

Rumex obtusifolius

leaves that were used to rear larvaeof

A. rumicis

had been washed in running water to removedust and foreign substances and then dried. The leaves of

R. obtusifolius

were cut equally around their main vein to asize of 1017.36 mm

2

with a sharp circular cutting device.First instar larvae were given one piece of leaf, second instarlarvae were given two pieces, and so on.

A growth chamber was used to rear larvae of

A. rumicis

at the constant temperature of 27

°

C, relative humidity of

75% and illumination of 12 000

±

100 Lux during the day,and 25

°

C, 75% and 0 Lux at night. The photoperiod wasmaintained at 14 h light : 10 h dark (LD 14:10). The filterpaper inside the Petri dish (100 mm diameter

×

15 mmheight) used to rear

A. rumicis

was changed every day. Thehumidity was maintained by adding 1 mL of first-stagedistilled water every day. The inside of each Petri dish wassterilized with 70% alcohol, cleaned with distilled waterand dried for reuse every day. When emergence of parasitestook place, 10% sucrose solution was provided throughcotton wool.

The life cycle of

G. liparidis

was studied using the groupof parasitoid larvae that had successfully completed lifecycles in the laboratory within the larvae of

A. rumicis

. Thenumber of egg bags left after the

G. liparidis

larvae had com-pleted their life cycles within 30 of the first through to fourthinstar larvae of

A. rumicis

was: four bags when fed first instarlarvae, 14 bags when fed second instar larvae, 22 bags whenfed third instar larvae and one bag when fed fourth instarlarvae. Thirty healthy larvae were picked from the groups offirst to fourth instars of

A. rumicis

and put into a plasticcontainer (8 cm wide

×

13 cm long

×

5 cm high) along with10 females and two males of

G. liparidis

that had emergedwithin 1 h previously. Each of them was parasitized byintroduction to

G. liparidis

for 5 h. The parasitizing test wasperformed once on the first and fourth instar larvae, and twiceon the second and third instar larvae. The subjects used formorphological measurements were 30 females from all theadults that had emerged from each bag of eggs. The bodylengths of the female

G. liparidis

did not include theirovipositors. Measurements were made using a stereo micro-scope (SMZ-2T; Nikon, Tokyo, Japan) and Image AnalysisSystem (BMI, version 4.0; BumMi Universe, Seoul, Korea).

All the statistical data were analyzed using

spss

Version 10.0(SPSS, Chicago, IL, USA). The life cycles of

G. liparidis

were verified using the non-parametric Kruskall-Wallis testwhile the parametric one-way

anova

test was used for themorphological characteristics of

G. liparidis

.

Results and discussion

Effect of host age on the life cycle of

G. liparidis

The life cycle of

G. liparidis

fed with each instar larvae of

A. rumicis

varied distinctly. When the first, second, third andfourth instar larvae were used as the food source, it tookeach instar larva of

G. liparidis

16.75

±

1.89, 15.00

±

2.43,13.96

±

0.33 and 11 days, respectively, from egg to cocoonproduction. These data show no large difference in the periodfrom egg to cocoon production per larval instar of

A. rumicis

.For

G. liparidis

emergence from pupa, it took 7.00

±

0.82days for first instar larvae, 6.70

±

0.57 days for second, 6.87

±

0.55 days for third and 8 days for fourth – these differences

Effect of host age on biology of

G. liparidis

Entomological Research

37

(2007) 103–107

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© 2007 The Authors. Journal compilation © 2007 The Entomological Society of Korea and Blackwell Publishing Asia Pty Ltd

are not significant. During the life cycle of

G. liparidis

fromegg to adult, there was a trend of declining time required fordevelopment of each succeeding instar; that is, 23.75

±

1.26days, 21.95

± 2.44 days, 20.83 ± 0.78 days and 19 days forinstars one to four (Fig. 1).

Oliveira et al. (1999) carried out experiments withG. liparidis and the closely related species Glyptapantelesmilitaris. By varying the instars (first to fourth) of Plutellaxylostella as hosts, the period from egg to larvae of the para-sitoids also varied from 23 to 16 days. Overall, there was abig difference in the life cycles of those feeding on differenthost instars, ranging from 31 to 24 days, in contrast to similarintervals required for pupation. In general, the life cycle ofparasitoids in older hosts is shorter (Allen 1990). This maybe due to the more abundant nutrition and space in the moremature host than in the young host (Vinson & Iwantsch 1980).

A parasitoid may suspend its development and continue asa first instar larva if the host is too small or unstable (Sato1980; Sato et al. 1986). This is understandable; a hasty attackwould likely cause the deaths of both the host and the para-sitoid owing to the host’s poor nutritional condition andcompromised immunity (Godfray 1994; Harvey et al. 1994;Mackauer et al. 1997). The first instar larva of A. rumicishad lower quantity and quality of food compared with that ofsecond or third instars. The koinobiont G. liparidis has toawait the growth of the first instar larva of A. rumicis whileliving in its body. For this reason, the growth of G. liparidisis accelerated in line with succeeding instars of A. rumicislarvae. But as shown by Oliveira et al. (1999), there is no

difference between the instars because the pupal state ofG. liparidis has neither an attack by G. liparidis nor adefense mechanism inside A. rumicis.

Effect of host age on morphological characteristics

of G. liparidis

It was found in the present study that the bodies of femaleG. liparidis were longer than those of males, except for thesecond instar, with a length of 2.57 ± 0.04 to 2.45 ± 0.10 mm,2.36 ± 0.20 to 2.28 ± 0.13 mm and 2.31 ± 0.08 to 2.20 ± 0.07 mmin the first, second and third instar after parasitizing instarlarvae of A. rumicis. The females had longer bodies, an averageof 2.41 ± 0.17 mm compared with the male average of 2.31± 0.14 mm. After being fed with the first, second and thirdinstar larvae of A. rumicis, the findings for the morphologicalcharacteristics were as follows (Fig. 2).

The female and male antenna lengths were 2.49 ± 0.06and 2.78 ± 0.06 mm for the first instars, 2.42 ± 0.19 and2.56 ± 0.12 mm for the second, and 2.47 ± 0.05 and 2.56 ±0.08 mm for the third. The antennae of males were clearlylonger than those of females. In terms of the female data byinstar, those fed with first instar larvae had the longest anten-nae, while there was no difference when fed second and thirdinstar larvae. The male parasitoid reared within a first instarhost had the longest antennae, in contrast to similar antennasizes found in those reared within second and third instarhosts (Fig. 3).

The female forewing length was longer than the malewith the results of 2.39 ± 0.06 to 2.31 ± 0.07 mm, 2.22 ±0.18 to 2.17 ± 0.11 mm and 2.21 ± 0.08 to 2.14 ± 0.06 mm,respectively (Fig. 4). The female forewing when fed the first

Figure 1 Developmental period (days + SD) of egg-cocoon, pupa-adult and egg-adult of Glyptapanteles liparidis at different host ages:�, first instar; �, second instar; , third instar; , fourth instar.Sample size was too small to be included in analysis in the fourthinstar group.

Figure 2 Body length (mm + SD) of Glyptapanteles liparidis male (�)and female (�) from Acronicta rumicis. Body lengths of all females(P < 0.001); body lengths of all males (P < 0.001); body lengthsbetween all females and males (P < 0.001). Sample size was toosmall to be included in analysis in the fourth instar group. Only femaleG. liparidis, which eat fourth instar larvae, appeared.

Y. Cho et al.

106 Entomological Research 37 (2007) 103–107 © 2007 The Authors. Journal compilation © 2007 The Entomological Society of Korea and Blackwell Publishing Asia Pty Ltd

instar was the longest. The average forewing length was2.27 ± 0.14 mm for the female and 2.21 ± 0.11 mm for themale (Fig. 4).

There was no great difference in head capsule widthbetween females and males except in the second instar, withthe results of 0.62 ± 0.01 to 0.64 ± 0.03 mm, 0.60 ± 0.03 to0.59 ± 0.04 mm and 0.59 ± 0.02 to 0.60 ± 0.02 mm (Fig. 5).Both males and females were found to have the widest headcapsules when fed first instar larvae. In general, there was nonotable difference between the male and female head capsulewidths (Fig. 5).

In conclusion, female G. liparidis that fed upon first instarhost larvae had superior body length, forewing length andhead capsule width compared with males, while the maleshad longer antennae. When fed second instar larvae, therewere no big differences in the body length and the head cap-sule width between the male and the female, however, themales had longer antennae while the females had longerforewings. In general, female body length and forewinglength surpass those of the male, while males have longerantennae. There was no difference in the head capsule widthbetween the two sexes. In the report of Kim (1970), thefemale body length was 3.2 ± 3.8 mm, compared to the male2.8 ± 3.2 mm. Similarly, the female forewing length was3.4 ± 4.0 mm, compared to the male 3.2 ± 3.6 mm. This doesnot appear to be a significant difference, in spite of thedeviation in the nominal size reported in the present work.The female has a longer body owing to the expanded abdomencontaining eggs, which is accompanied by the enlargedforewing. The better developed antennae in the male makessense because the males use the antennae to detect thefemale’s position for mating (Quicke 1997).

Mirchev et al. (2001) reported that the forewing lengthof male and female Pimpla nipponica increased in proportionto the weight of Galleria mellonella, its host. Bernal et al.(2001), Harvey et al. (1994) and Paine et al. (2004) reportedthat the tibiae of the female and male parasitoid’s hind legslengthened according to the host’s size or weight. That is, itappeared that the size of the adult parasitoid was determinedby the amount and quality of the food that the larvae ate. Inthe present study, the first instar larvae of A. rumicis assumeda role in rearing a longer body, forewing and antenna and awider head capsule for both male and female G. liparidis. This

Figure 3 Antenna length (mm + SD) of Glyptapanteles liparidismale (�) and female (�) on Acronicta rumicis. Antenna length of allfemales (P = 0.034); antenna length of all males (P < 0.001);antenna length between all females and males (P < 0.001). Samplesize was too small to be included in analysis in the fourth instar group.Only female G. liparidis, which eat fourth instar larvae, appeared.

Figure 4 Forewing length (mm + SD) of Glyptapanteles liparidismale (�) and female (�) on Acronicta rumicis. Forewing length of allfemales (P < 0.001); forewing length of all males (P < 0.001);forewing length between all females and males (P = 0.001). Samplesize was too small to be included in analysis in the fourth instar group.Only female G. liparidis, which eat fourth instar larvae, appeared.

Figure 5 Head capsule width (mm + SD) of Glyptapanteles liparidismale (�) and female (�) on Acronicta rumicis. Head capsule widthof all females (P < 0.001); head capsule width of all males (P < 0.001);head capsule width between all females and males (P = 0.211). Samplesize was too small to be included in analysis in the fourth instar group.Only female G. liparidis, which eat fourth instar larvae, appeared.

Effect of host age on biology of G. liparidis

Entomological Research 37 (2007) 103–107 107© 2007 The Authors. Journal compilation © 2007 The Entomological Society of Korea and Blackwell Publishing Asia Pty Ltd

result implies that G. liparidis oviposits fewer eggs in thefirst instar larvae of A. rumicis than in the second or the thirdinstars, and has a longer life cycle, but that G. liparidis adultsfed with the first instar larvae emerge with morphologicalcharacteristics far superior to those fed with second and thirdinstar larvae and have a unique reproductive strategy.

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