ecological and morphological characteristics of endoparasitoids on elcysma westwoodii (vollenhoven)...

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SHORT COMMUNICATION Ecological and morphological characteristics of endoparasitoids on Elcysma westwoodii (Vollenhoven) (Lepidoptera: Zygaenidae) Youngho CHO 1 *, Youngjin KIM 1 *, Yong-Gu HAN 1 , Young Kook KANG 1 , Minjoo CHOI 1 , Heonmyoung LIM 2 , Youngjun PARK 2 and Sang-Ho NAM 1 1 Department of Biology, Daejeon University, Daejeon, Korea 2 Ecosystem Assessment Division, Ecology Research Department, National Institute of Environmental Research, Incheon, Korea Correspondence Sang-Ho Nam, Department of Biology, Daejeon University, Daejeon, Korea. Email: [email protected] Received 20 April 2010; accepted 22 June 2010. *These authors contributed equally to this paper. doi: 10.1111/j.1748-5967.2010.00292.x Abstract Six species of insect endoparasitoids were identified from Elcysma westwoodii, which is the most damaging lepidopteran pest of Prunus yedoensis. From Hymenoptera, two species were identified: a species in Braconidae and Charops striatus in Ichneumonidae. From Diptera, there were four species in Tachinidae: Compsilura concinnata, Exorista sp., Pales sp. and Tachinidae spp. The parasitic ratio was 4.86% (45 of 926 larvae). The hymenopterans were parasitic on 31 individuals of E. westwoodii (68.9%) and the dipterans were parasitic on 14 individuals (31.1%). It was found that parasitoids from the larvae of E. westwoodii were all either endoparasitoids or larval parasitoids. However, Exorista sp. of Tachinidae was found to be either a larval parasitoid or larval-pupal parasitoid. Additionally, all the identified parasitoids were solitary parasitoids, as only one parasite occurred in a larva of E. westwoodii. Because the larva of E. westwoodii eats and molts after it is parasitized, all the parasitoids were identified as koino- bionts. There were no big differences in morphological characteristics and life histories between C. striatus and C. concinnata. However, for Exorista sp. and Pales sp., males took 3–5 days longer to emerge from their pupae and had remark- ably longer body lengths than females. Key words: Braconidae, Elcysma westwoodii, Endoparasiotoid, Ichneumonidae, Tachinidae. Introduction Although there was an outbreak of Elcysma westwoodii in Prunus yedoensis in the Gyeryong Mountain National Park in 2000 (Figs 1,2), there have not been effective measures against the pest because of two conflicting purposes of the National Park: the preservation of biodiversity and the pro- vision of comfort for visitors. Elcysma westwoodii (Lepidoptera: Zygaenidae: Chal- cosiinae) inhabits all areas of South Korea and occurs in Japan, China, East Russia, India and Nepal. Adults occur once a year, typically from September to October. They mainly fly around the food plants in the daytime and are attracted by lights at night (Shin et al. 1983; Lee & Chung 1997; Shin 2001). The head and thorax of E. westwoodii larvae are black, the venter of the abdomen is white; the dorsum of the abdomen is yellow with black stripes (Mutuura et al. 1975). Larvae emerge in April, are in the last larval period by the end of June and become pupa after a 50-day prepupal period (Mutuura et al. 1975; Lee & Chung 1997). Larvae eat the leaves of more than 10 species of plants including Prunus spp., Malus pumila var. dulcissima and Chaenomeles lagenariae (Shin et al. 1983; Esaki et al. 1999). When these larvae emerge, only the stems are left in the food plants (Shin 2001). The deciduous broad-leaved Entomological Research 40 (2010) 270–276 © 2010 The Authors Entomological Research © 2010 The Entomological Society of Korea and Blackwell Publishing Asia Pty Ltd

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Page 1: Ecological and morphological characteristics of endoparasitoids on Elcysma westwoodii (Vollenhoven) (Lepidoptera: Zygaenidae)

SHORT COMMUNICATION

Ecological and morphological characteristics ofendoparasitoids on Elcysma westwoodii (Vollenhoven)(Lepidoptera: Zygaenidae)Youngho CHO1*, Youngjin KIM1*, Yong-Gu HAN1, Young Kook KANG1, Minjoo CHOI1,Heonmyoung LIM2, Youngjun PARK2 and Sang-Ho NAM1

1 Department of Biology, Daejeon University, Daejeon, Korea2 Ecosystem Assessment Division, Ecology Research Department, National Institute of Environmental Research, Incheon, Korea

Correspondence

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

Received 20 April 2010;accepted 22 June 2010.

*These authors contributed equally to thispaper.

doi: 10.1111/j.1748-5967.2010.00292.x

Abstract

Six species of insect endoparasitoids were identified from Elcysma westwoodii,which is the most damaging lepidopteran pest of Prunus yedoensis. FromHymenoptera, two species were identified: a species in Braconidae and Charopsstriatus in Ichneumonidae. From Diptera, there were four species in Tachinidae:Compsilura concinnata, Exorista sp., Pales sp. and Tachinidae spp. The parasiticratio was 4.86% (45 of 926 larvae). The hymenopterans were parasitic on 31individuals of E. westwoodii (68.9%) and the dipterans were parasitic on 14individuals (31.1%). It was found that parasitoids from the larvae of E. westwoodiiwere all either endoparasitoids or larval parasitoids. However, Exorista sp. ofTachinidae was found to be either a larval parasitoid or larval-pupal parasitoid.Additionally, all the identified parasitoids were solitary parasitoids, as only oneparasite occurred in a larva of E. westwoodii. Because the larva of E. westwoodiieats and molts after it is parasitized, all the parasitoids were identified as koino-bionts. There were no big differences in morphological characteristics and lifehistories between C. striatus and C. concinnata. However, for Exorista sp. andPales sp., males took 3–5 days longer to emerge from their pupae and had remark-ably longer body lengths than females.

Key words: Braconidae, Elcysma westwoodii, Endoparasiotoid, Ichneumonidae, Tachinidae.

Introduction

Although there was an outbreak of Elcysma westwoodii inPrunus yedoensis in the Gyeryong Mountain National Parkin 2000 (Figs 1,2), there have not been effective measuresagainst the pest because of two conflicting purposes of theNational Park: the preservation of biodiversity and the pro-vision of comfort for visitors.

Elcysma westwoodii (Lepidoptera: Zygaenidae: Chal-cosiinae) inhabits all areas of South Korea and occurs inJapan, China, East Russia, India and Nepal. Adults occuronce a year, typically from September to October. Theymainly fly around the food plants in the daytime and are

attracted by lights at night (Shin et al. 1983; Lee & Chung1997; Shin 2001). The head and thorax of E. westwoodiilarvae are black, the venter of the abdomen is white; thedorsum of the abdomen is yellow with black stripes(Mutuura et al. 1975). Larvae emerge in April, are in the lastlarval period by the end of June and become pupa after a50-day prepupal period (Mutuura et al. 1975; Lee & Chung1997).

Larvae eat the leaves of more than 10 species of plantsincluding Prunus spp., Malus pumila var. dulcissima andChaenomeles lagenariae (Shin et al. 1983; Esaki et al.1999). When these larvae emerge, only the stems are left inthe food plants (Shin 2001). The deciduous broad-leaved

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tree P. yedoensis, the major food plant of E. westwoodiilarvae, is widely planted in Korea as it has beautiful flowers(Kim 1998). Although most Prunus species, includingPrunus yedoensis, are economic tree species, studies on thepests of these species are insufficient. Recently, Lee et al.(2006) recorded Pseudaulacaspis prunicola, Myzus persicaeand Synanthedon hector as harmful insects to P. yedoensis.In studies on pests of related trees, Kim et al. (2007) discov-ered 10 species, Kim and Kim (1999) found 32 species andLee and Chung (1997) recorded 410 species. There havebeen few scientific records of the pests of P. yedoensis.However, we can say it is the commercial tree species thattend to be more seriously damaged by pests. There are over410 species of pests known to damage commercial trees.With recorded infestations in both Korea and Japan (Yuki-nari 2001) there is always potential for additional largeoutbreaks.

The purpose of this article is to identify possible biologi-cal control agents for E. westwoodii larvae occurring in P.yedoensis from April to June. This study investigated thekinds of parasitoid insects using E. westwoodii, along withtheir ecological and biological characteristics and parasiticratios.

Materials and methods

In order to check them for parasitoids, 926 individuals of E.westwoodii larvae were collected in the Gyeryong MountainNational Park from April to May 2005. The collected larvaewere reared in a growth chamber at 27°C, 70% relativehumidity (RH) under conditions of 14 h light : 10 h dark(LD 14:10). Each larva was grown in a Petri dish (100 mmdiameter ¥ 15 mm height) with the filter paper (85 mm;Whatman no. 2; Whatman, Maidstone, Kent, UK) liningchanged every day. The humidity was maintained with 1 mLdistilled water. Excretions were removed daily from thePetri dish, which was then sterilized with 70% alcohol,rinsed with distilled water and then dried.

For feeding, P. yedoensis leaves free from agriculturalchemicals were used. Leaves clearly affected by other insectgroups, viruses or bacteria were excluded. The selectedleaves were washed in running water to remove dust andother foreign substances and then dried before use. Leaveswere supplied constantly, even after the parasitoids escapedfrom the larvae, to monitor the feeding activities of thelarvae after the exit of the parasitoids. The rearing conditionsof the parasitoids were the same as those of host insects.When parasitoids exited their hosts, a cotton ball soaked in10% sucrose solution was supplied to check the longevity ofthe parasitoids. The major axis, minor axis and body lengthof the endoparasitoids in E. westwoodii were measuredusing an image analysis system (BMI, v4.0; BumMi Uni-verse, Seoul, Korea).

Results and discussion

Species composition of parasitoids and

parasitic ratio

Six species of parasitoids of E. westwoodii were found tooccur in two insect orders and three families (Table 1).These included two hymenopteran species (Braconidae spp.,C. striatus of Ichneumonidae) and four dipteran species(Tachinidae: C. concinnata, Exorista sp., Pales sp., Tachin-idae spp.).

The Braconidae species is being identified at present andgenus Charops was recorded in Korea very recently by Choiand Lee (2008). It used to be recorded as C. bicolor only andChoi and Lee (2008) discovered its habitat in Korea for thefirst time. Charops striatus inhabits the eastern Palaearcticand Oriental regions. In this work, we discovered for the firsttime that E. westwoodii is its host insect. Compsilura con-cinnata is a well-known dipteran parasitoid of Lymantriadispar. It is polyphagous, having host insects more than 100species of which are identified in the Palaearctic region(Herting 1960), 161 in North America (Arnaud 1978) and 59

Figures 1–2 1 Prunus yedoensis damagedby Elcysma westwoodii larvae; 2 E. west-woodii larva.

Endoparasitoids on Elcysma westwoodii

271Entomological Research 40 (2010) 270–276© 2010 The Authors. Entomological Research © 2010 The Entomological Society of Korea and Blackwell Publishing Asia Pty Ltd

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in Japan (Shima 1999). It was first confirmed in Korea as aparasitoid of E. westwoodii. Exorista sp. is a well-knownparasitoid of Tachinidae (Hirose 2005). A related species, E.sorbillans, is a representative parasitoid of Bombyx mori. InJapan, 46 species have been reported as hosts of E. japonica,another related species (Kan et al. 2003). In Korea, only twospecies in genus Exorista have been recorded (E. japonica,E. sorbillans) (ESK & KSAE 1994). Recorded hosts includeMalacosoma neustria, Euproctis subflava, L. dispar, Bar-athra brassicae, Hyphantria cunea and Dictyoplocajaponica (Paik et al. 1981). Here, for the first time, E. west-woodii is confirmed as a new host of a species in genusExorista. Before now, Pales sp. had not been recorded inKorea. It is a representative parasitoid of B. mori and eachlarva lays 1000 to 2000 eggs on the undersurface of mul-berry leaves (Hirose 2005). Members of genus Pales areknown as polyphagous insects that parasitize lepidopteransand include around 70 species worldwide (Cerretti 2005). InJapan, 42 species including H. cunea have been reported(Shima 1999). In this work, Pales sp. is identified as a newparasitoid of E. westwoodii with the aforementioned twotachinid species.

The parasitic ratio on the E. westwoodii larvae was iden-tified as 4.86% (Table 1). The parasitic ratio of Hymenopterawas 3.35%, which is more than twice that of Diptera(1.51%). It shows that parasitic wasps occupy more than80% of the total parasite insects and become general para-sites (Quicke 1997). The parasitic ratio of braconid waspswas 1.30% (12 of 926 individuals) while that of C. striatusfrom ichneumonid wasps was 2.05% (19 of 926 individuals).The parasitic ratios of Diptera were 0.32%, 0.54%, 0.32%and 0.32% for C. concinnata, Exorista sp., Pales sp. andTachinidae spp, respectively. Elcysma westwoodii can beclassified as an oligophagous insect as it uses more than 10kinds of feeding plants. The parasitic ratio on E. westwoodiilarvae was 4.86%. This is a relatively low rate compared to40.8% and 22.97% of L. dispar and Acronicta rumicis,respectively, although they can not be compared directly

with E. westwoodii because they are polyphagous insects(Hoch et al. 2001; Cho 2004). It seems that E. westwoodiihas a lower parasitic ratio compared to polyphagous insects,which have around 50 to 100 feeding plants, because it isonly exposed to parasitic insects on approximately ten kindsof feeding plants.

Ecological characteristics of parasitoids

Braconidae spp. and C. striatus, the parasitic wasps on E.westwoodii larvae, are verified as endoparasitoids (Table 2).Elcysma westwoodii larvae feed and molt even after exit ofthe parasitic wasps. Therefore, both Braconidae spp. and C.striatus are koinobionts. Additionally, they are solitaryparasitoids as only one individual uses each E. westwoodiilarva.

Compsilura concinnata, Exorista sp., Pales sp. andTachinidae spp. (all tachinid parasitoids of E. westwoodiilarvae) are identified as koinobionts and solitary parasitoids(Table 2). However, C. concinnata is a polyphagous parasi-toid that has more than 100 species of host insects (Herting1960). It is a representative parasitoid on macrolepidopterouslarvae, in particular on L. dispar. It is known as a gregariousparasitoid on L. dispar (Kenis & Vaamonde 1998). Thereason for this gregarious activity is not consistent with theresults of this study, perhaps because E. westwoodii larvae arenot as big as L. dispar larvae and may not provide adequatefood for groups of C. concinnata larvae. It is guessed that thisrestricts egg laying and maintains the solitary life cycle of C.concinnata in hosts like E. westwoodii.

Among the Tachinidae found in E. westwoodii larvae,only Exorista sp. is a larval and larval–pupal parasitoid,while C. concinnata, Pales sp. and Tachinidae spp. are alllarval parasitoids. Yasumatsu and Watanabe (1964)reported that E. japonica, E. rustica and E. sorbillans arelarval parasitoids. However, in this study, the larvae ofExorista sp. emerged both in E. westwoodii larvae andprepupa, which makes Exorista sp. both a larval and larval-

Table 1 Parasitism by parasitoids on Elcysma westwoodii

Order Family Species P.A/C.I

Parasitism (%)

Species Order Total

Hymenoptera Braconidae Braconidae spp. 12/926 1.30 3.35 4.86Ichumonidae Charops striatus 19/926 2.05

Diptera Tachinidae Compsilura concinnata 3/926 0.32 1.51Exorista sp. 5/926 0.54Pales sp. 3/926 0.32Tachinidae spp. 3/926 0.32

C.I, collected individuals from E. westwoodii; P.A, parasitoid appearance on E. westwoodii.

Y. Cho et al.

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pupal parasitoid. Further research is needed to determinewhether Exorista sp. larvae exit the host later because ofthe nutritional condition of the host, or because the Exoristasp. used in this study have different ecological characteris-tics from those existing, closely related species for whichresults have been reported.

In this experiment, C. concinnata is confirmed as a larvalparasitoid. However, Cho et al. (2006) recorded C. concin-nata as a larval–pupal parasitoid on A. rumicis, just asYasumatsu and Watanabe(1965) recorded C. concinnata aslarval–pupal parasitoids on Canephora asiatica, L. dispar,Inachis io, Parasa consocia, Pieris melete, P. rapae andTansima marginalis. Additionally, Yang et al. (2008)recorded C. concinnata as a pupal parasitoid on H. cunea. Asmentioned above, it seems that C. concinnata can be a larval,larval–pupal or pupal parasitoid according to the type andnutrient status of the host.

Morphological characteristics and life cycles

of parasitoids

With regard to C. striatus, the time for development of thepupa and emergence of an adult was similar in males andfemales (8.29 � 0.49, 8.50 � 0.53 days, respectively). Thelife spans of adult males and females were 2.57 � 0.53 and2.88 � 0.99 days, respectively. The major axes and minoraxes of male and female pupae were 5.54 � 0.34 mm/2.59� 0.19 mm and 5.54 � 0.52 mm/2.57 � 0.27 mm, respec-tively, which was not significantly different. The bodylengths of males and females were not significantly different(7.86 � 0.5, 7.97 � 0.99 mm, respectively (Table 3, Fig. 3).

With regard to C. concinnata, the period from pupa toadult was similar in males and females (13.14, 14.00 days,respectively). The life spans of adult males and females were2.5 � 0.71 and 3.00 days, respectively. The major axes and

Table 2 Ecological characteristics of endoparasitoids of Elcysma westwoodii larvae

Parasitizedhoststage

Parasitoidescape stage

Parasitizedhost

ecdysisFood consumption of

parasitized hostSolitary (S) orgregarious (G)

Idiobiont (I) orkoinobiont (K)

HymenopteraBraconidae

Braconidae spp. Larva Larva Yes Yes S KIchumonidae

Charops striatus Larva Larva Yes Yes S KDiptera

TachinidaeCompsilura concinnata Larva Larva Yes Yes S KExorista sp. Larva Larva or prepupa Yes Yes S KPales sp. Larva Larva Yes Yes S KTachinidae spp. Larva Larva Yes Yes S K

Table 3 Ecological characteristics of Charops striatus, Compsilura concinnata, Exorista sp. and Pales sp

�/�Time of cocoon (pupa) to

adult (days)Longevity of parasitoids in

adult stage (days)Size of cocoon(pupa) (mm)

Major axis/Minor axis Body length (mm)

HymenopteraIchumonidae

Charops striatus � 8.29 � 0.49 2.57 � 0.53 5.54 � 0.34/2.59 � 0.19 7.86 � 0.5� 8.50 � 0.53 2.88 � 0.99 5.54 � 0.52/2.57 � 0.27 7.97 � 0.99

DipteraTachinidae

Compsilura concinnata � 13.14 2.5 � 0.71 6.27 � 0.69/3.13 � 0.33 7.55 � 0.81� 14 3 7.16/3.58 8.04

Exorista sp. � 13 3 6.05/2.84 7.57� 9.75 � 0.5 3.25 � 0.5 4.16 � 0.48/2.06 � 0.2 4.77 � 0.61

Pales sp. � 10.5 � 0.71 3 6.15 � 0.05/2.74 � 0.16 7.06 � 0.1� 5 5 4.43/2.26 5.68

Endoparasitoids on Elcysma westwoodii

273Entomological Research 40 (2010) 270–276© 2010 The Authors. Entomological Research © 2010 The Entomological Society of Korea and Blackwell Publishing Asia Pty Ltd

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minor axes of male and female pupae were 6.27 � 0.69 mm/3.13 � 0.33 mm and 7.16 mm/3.58 mm, respectively, whichdoes not show significant difference between males andfemales. The body lengths of males and females were notsignificantly different at 7.55 � 0.81 and 8.04 mm, respec-tively (Table 3, Fig. 4). Results from this study differ fromprevious studies. Cho et al. (2006) reported the body lengthof female C. concinnata parasitizing a A. rumicis larva as9.5 mm, and Yasumatsu et al. (1976) reported the bodylength of C. concinnata adults as 8–10 mm. It may be thatthe growth of C. concinnata larvae depends on the size andage of the host insect larva.

With regard to Exorista sp., the interval from pupa to adultwas a little different in males and females, at 13.00 and 9.75� 0.50 days, respectively. It was also found that femalesemerged approximately three days earlier than males. Thelifespan of adult males and females was 3.00 and 3.25 � 0.5days, respectively. The major axes and minor axes of maleand female pupae were 6.05 mm/2.84 mm and 4.16 �

0.48 mm/2.06 � 0.2 mm, respectively, which means malepupae are larger. The body lengths of male and female adultinsects were 7.57 mm and 4.77 � 0.61 mm, respectively,which shows males have longer body lengths than females(Table 3, Fig. 5).

With regard to Pales sp., the intervals from pupa to adultof males and females were 10.5 � 0.71 and 5 days, respec-tively. Males take twice as long as females. The life spans of

adult males and females were 3 and 5 days, respectively. Themajor axes and minor axes of male and female pupae were6.15 � 0.05 mm/2.74 � 0.16 mm and 4.43 mm/2.26 mm,respectively. The body lengths of male and female adultswere 7.06 � 0.1 and 5.68 mm, respectively (Table 3, Fig. 6).With regard to a P. pavida adult, which is a closely relatedspecies, the body lengths of the male and female adults were7.2–9.0 and 9.0–9.5 mm when the host was B. mori (Hirose2005). This is very different from the result of this study.However, in P. abdita, another closely related species, thebody length of male adult was 6.3–10.2 mm and in P. marae,6.3–9.1 mm, both of which show large differences fromgenus Pales. In summary, it seems that the body length ofthe adult Pales sp. depends on how well it has used thehost’s resources during its larval period.

Conclusion

In Korea, Prunus yedoensis is very popular and widelyplanted as street plants to support many Cherry BlossomFestivals such as those at Jin-hae and Yeouido. As there areplenty of plants upon which to feed, large outbreaks of E.westwoodii, which feeds on Prunus spp., are possible at anytime. Therefore in-depth studies on biological, physical andchemical control methods are greatly needed. In this experi-ment, it was found that tachinid flies could not be used asbiological agents because they are polyphagous parasitoids

Figures 3–6 Endoparasitoids of Elcysmawestwoodii larvae. 3 Charops striatus(female); 4 Compsilura concinnata (female);5 Exorista sp. (female); 6 Pales sp. (male).

Y. Cho et al.

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that feed on a diverse group of plants. However, in the caseof C. striatus, its host insects are not well known. Up to now,only Balataea funeralis, a host that is a major pest ofbamboo and reported by Yu and Horstmann (1997) and E.westwoodii reported in this study are the only known hostinsects. Additionally, all of the known host insects of C.striatus belong to the lepidopteran family Zygaenidae,which is perceived as harmful. Given this finding, C. striatusappears to be a specialist parasitoid of zygaenid species.Although further studies should be done, it seems now thatthere is a high probability that C. striatus could be used as abiological control agent for E. westwoodii.

Acknowledgements

This study was supported by the Korean Institute of Envi-ronmental Science and Technology, Ministry of Environ-ment grant (KIEST 052-081-072).

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