parasitic hymenoptera reared from the insects on...

E. KOÇAK, M. ÖZDEMİR

201

Turk J Zool

2012; 36(2): 201-208

© TÜBİTAK

doi:10.3906/zoo-1008-129

Parasitic Hymenoptera reared from the insects on

Heracleum platytaenium Boiss. (Apiaceae) with new faunistic

and biological records

Erhan KOÇAK1,

*, Mustafa ÖZDEMİR2

1Department of Agricultural Biotechnology, Faculty of Agriculture, Süleyman Demirel University, Isparta - TURKEY

2Plant Protection Central Research Institute, Yenimahalle, Ankara - TURKEY

Received: 24.08.2010

Abstract: Some parasitic hymenopterans were reared from their host insects found on the stems and branches of

Heracleum platytaenium Boiss., which contains furanocoumarins that are insect repellents and suppress growth in

some species. Plant materials with insects were collected from the vicinity of Kızılcahamam in Ankara Province in

July-September 2008. Th e parasitoids (Hymenoptera) and their hosts were Didyctium brunnea (Belizin) (Eucolidae)

from puparia of Lasiambia albidipennis (Strobl) (Diptera: Chloropidae), Pronotalia carlinarum (Szelenyi & Erdos)

(Eulophidae) and Homoporus febriculosus (Girault) (Pteromalidae) from puparia of Melanagromyza heracleana Zlobin

(Diptera: Agromyzidae), and Baryscapus crassicornis (Erdos) (Eulophidae) from larvae, pupae, and adults of Lixus

nordmanni Hochhuth (Coleoptera: Curculionidae). Th e hole(s) or cutting types done by the parasitoids while leaving

their hosts were described. Development time from egg to adult (12 days and 19-20 days) and parasitization duration (60

min and 20-30 min) were also determined for P. carlinarum and B. crassicornis, respectively, and average parasitization

rates in nature and the mating behaviors of these 2 parasitoids were defi ned. To our knowledge, the insects are new hosts

for all parasitoids and the fi rst parasitoid records for the fl ies. Chloropidae is a new record host family for D. brunnea

aft er Phoridae. In addition, D. brunnea and H. febriculosus were recorded from Turkey for the fi rst time.

Key words: Baryscapus, Didyctium, Homoporus, Pronotalia, Lixus, Lasiambia, Melanagromyza, Heracleum, new records,

Turkey

Biyolojik ve faunistik yeni kayıtlarla Heracleum platytaenium Boiss. (Apiaceae)

üzerindeki böceklerden elde edilen parazitoitler

Özet: Bu çalışmada bazı böceklere repellent etkisi olan ve büyümeyi engelleyen bir madde olan kumarin içeren bir

bitki olan Heracleum platytaenium Boiss.’un gövde ve saplarının içerisinde beslenen bazı coleopter ve dipterlerin

Hymenoptera takımından parazitoitleri elde edilmiştir. Bitki materyali böceklerle birlikte Ankara’nın Kızılcahamam

ilçesinden Temmuz-Eylül 2008 döneminde toplanmıştır. Elde edilen parazitoidlerden Didyctium brunnea (Belizin)

(Eucolidae), Lasiambia albidipennis (Strobl) (Diptera: Chloropidae) pupalarından; Pronotalia carlinarum (Szelenyi

& Erdos) (Eulophidae) ve Homoporus febriculosus (Girault) (Pteromalidae), Melanagromyza heracleana Zlobin

(Diptera: Agromyzidae) pupalarından ve Baryscapus crassicornis (Erdos) (Eulophidae) ise Lixus nordmanni Hochhuth

Research Article

* E-mail: [email protected]

Parasitic Hymenoptera reared from the insects on Heracleum platytaenium Boiss. (Apiaceae) with new faunistic and biological records

202

Introduction

Th e genus Heracleum L. (Apiaceae) includes approximately 125 species worldwide and 23 in Turkey (Pimenov and Leonov, 2004). Heracleum platytaenium Boiss. is a perennial herbaceous and monocarpic endemic species belonging to the Euxine phytogeographic region (Davis, 1972) and it yields furanocoumarins (Nielsen, 1970), which are known to be insect repellents and suppress the growth of some insect species (Berenbaum, 1981; Moore and Debboun, 2006). So far, many studies have been carried out on the insects of Heracleum species in the world, especially on their biology and natural enemies (Burki and Nentwig, 1997; Hansen et al., 2006; Hattendorf et al., 2006; Page et al., 2006; Koçak et al., 2009). In this study, the parasitoids were inspected on Lixus nordmanni Hochhuth (Coleoptera: Curculionidae), Melanagromyza heracleana Zlobin (Diptera: Agromyzidae), and Lasiambia albidipennis (Strobl) (Diptera: Chloropidae) from the stems and branches of H. platytaenium.

As for the host insects, the genus Lixus is wildly distributed worldwide and comprises over 500 species, with over 150 species in the Palaearctic region (Csiki, 1934; Ter-Minassian, 1967). L. nordmanni is distributed in the Caucasus (Petri, 1904/1905) and Turkey (Gültekin, 2006; Koçak et al., 2009). Th is species feeds on Heracleum species (Gültekin, 2006). Some Lixus species are actual agricultural pests (Nikulina, 1989; Volovnik, 1994), and some can potentially be used for biological control of weeds (Gültekin, 2004). Chlorocytus longicauda (Th .) (Hymenoptera: Pteromalidae) was reared from the pupal stage of Lixus nordmanni by Gültekin (2006).

Th e Lasiambia Sabrosky genus consists of 12 species in Europe. L. albidipennis is a little-known

and rare species recorded form Croatia, France, Italia, southern Russia, and the Czech Republic (Kubik, 2006) and Turkey (Koçak et al., 2009). Th is species is known as saprophagous (Nartshuk, 2005) and its larvae are generally found near or on decomposed stems, caused by some larvae of L. nordmanni and M. heracleana. Moreover, the larvae feed inside the dead bodies of L. nordmanni larvae or pupae (Koçak et al., 2009).

Melanagromyza Hendel is among the largest genera of the family Agromyzidae, representing 357 species in the world fauna. Th eir primary feeding habit is internal stem-boring in Apiaceae. M. heracleana was recorded as stem-borers in Heracleum mantegazzianum Sommier & Levier in Russia (Zlobin, 2005) and H. platytaenium in Turkey (Koçak et al., 2009).

Although there are some records of parasitoids of some species of the genera Lasiambia and Melanagromyza, there are no parasitoid records on L. albidipennis or M. heracleana.

In the present paper, we report on new faunistic studies, biological data on parasitoids, and host-parasitoid relationships.

Materials and methods

Heracleum platytaenium specimens were collected in the vicinity of Kızılcahamam (between 40°33ʹN and 40°30ʹN and 32°33ʹE and 32°38ʹE, approximately 1000 m a.s.l.), in Ankara Province in July-September 2008. Plants including the diff erent stages of insects were collected. In the insectariums, the stems were investigated and kept separate from the umbels (seeds and fl ower stalks) in diff erent cabins. Th e diff erent insect species were separated individually

(Coleoptera: Curculionidae) larva, pupa ve erginlerinden elde edilmiştir. Parazitoitlerin konukçularını terk ederken

meydana getirdikleri delikler ve kesme tipleri tanımlanmıştır. Ayrıca, P. carlinarum ve B. crassicornis için sırasıyla

yumurtadan ergine gelişme sürelerinin 12 gün ve 19-20 gün ve parazitleme sürelerinin 60 dakika ve 20-30 dakika olması

gibi bazı biyolojik parametreler belirlenmiştir. Bu 2 türün doğadaki parazitleme oranları ortaya konmuş, ayrıca çift leşme

davranışları da tanımlanmıştır. Çalışmadaki böceklerin tümü parazitoidler için yeni konukçu olup bu çalışmadaki

dipterlerin ise ilk parazitoit kayıtları olmuştur. Chloropidae familyası D. brunnea için Phoridae familyasından sonra

yeni konukçu olarak kaydedilmiştir. D. brunnea ve H. febriculosus türleri Türkiye faunası için yeni kayıt durumundadır.

Anahtar sözcükler: Baryscapus, Didyctium, Homoporus, Pronotalia, Lixus, Lasiambia, Melanagromyza, Heracleum, yeni

kayıtlar, Türkiye


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into diff erent developmental stages in small cut stem parts. Parasitization rates were also determined according to the number of parasitized individuals among all individuals brought in from the fi eld.

Biological studies were carried out for P. carlinarum on puparia of M. heracleana and for B. crassicornis on larva of L. nordmanni at 25 ± 1 °C and 70 ± 5% RH with a photoperiod of 16:8 (L:D) in a climate chamber. Th e parasitoid adults were fed with honey. In total, 4 host insect specimens were used for parasitization separately for both parasitoids. In July, the fourth stages of Lixus larvae collected on plant stems were separated and observed for 3 days to be sure they were not parasitized by any parasitoid. Similar observations for both parasitization and development of adult fl ies were conducted during 1 week for overwintering M. heracleana puparia collected at the end of September. General mating behavior of the parasitoids in petri dishes was observed and easily noted with the naked eye. Th ree repetitions with 3 diff erent couples of parasitoids were done on the same day for each parasitoid species under laboratory conditions.

A pteromalid specimen was identifi ed using the identifi cation key of Dzhanokmen (1987).

All specimens used in this study were deposited at the Plant Protection Central Research Institute in Ankara, Turkey, except for 2 males and 2 females of D. brunnea that are at the Department of Systematic Zoology, Uppsala University, Sweden.

Results and discussion

In the current study, parasitic wasps and their hosts on H. platytaenium were determined to be Didyctium brunnea (Belizin) (Eucolidae) from L. albidipennis, Pronotalia carlinarum (Szelenyi & Erdos) (Eulophidae) and Homoporus febriculosus (Girault) (Pteromalidae) from M. heracleana, and Baryscapus crassicornis (Erdos) (Eulophidae) from L. nordmanni. None of the parasitoids of the fl ies M. heracleana and L. albidipennis were known on these hosts. Previously, a pteromalid pupal parasitoid (C. longicauda) of L. nordmanni was described from Turkey (Gültekin, 2006).

Two eulophid species, B. crassicornis and P. carlinarum from Tetrastichinae, were reared from

the weevil L. nordmanni and fl y M. heracleana, respectively. Gibson (1993) found that Tetrastichinae species were mostly internal primary parasitoids of the eggs, larvae, or pupae of Lepidoptera, Coleoptera, and Diptera, but they have been reared from members of 10 insect orders, and a few species are phytophagous, predaceous on gall mites (Acari), or parasitoids of thrips larvae (Th ysanoptera). Tetrastichines are equally diverse in other aspects of their biology, such that few generalizations can be made about the group as a whole. Species can be solitary or gregarious, primary or secondary parasitoids, and monophagous to polyphagous. Although they predominantly attack larvae or pupae, many egg parasitoids are known, and a few are even parasitoids of adults (LaSalle and Boler, 1994).

Lixus nordmanni is a newly recorded host for B. crassicornis (Figure 1). Th e parasitoid was reared as an endoparasitoid from larvae of various stages, pupae, and adult stages of L. nordmanni. Diff erent stages of L. nordmanni (72 adults, 41 pupae, and 35 larvae) were obtained and their parasitization rates were determined to be 15.2%, 14.6%, and 28.5%, respectively, with an average parasitization of 18.9%. Th e adult wasps emerge through a few circular holes from diff erent parts of the body. H. platytaenium is a new host plant for this parasitoid. B. crassicornis was described from Asteraceae on Larinus species (Coleoptera: Curculionidae) (Domenichini, 1966; Graham, 1991) and Tephritis conycifoliae (Diptera: Tephritidae) (Vidal, 1997). Yegorenkova (2008) recorded B. endophiticus (Dominichini) from Lixus iridis Olivier (Coleoptera: Curculionidae) on Satureja hortensis (Labiatae). Doganlar (1993) determined the parasitoid from Onopordon sp. (Asteraceae) as the fi rst record in Turkey. Recently, a pteromalid parasitoid, C. longicauda, was reared from L. nordmanni on Heracleum sp. in Turkey (Gültekin, 2006). In the present study, B. crassicornis females paralyzed the L. nordmanni larva and later oviposited into the larvae over the course of 20-30 min. It is an idiobiont parasitoid that paralyzes the host permanently. It required 19-20 days to complete development from egg to adult. A maximum of 52 specimens (9 males and 43 females) and a minimum of 18 specimens (3 males and 15 females) were reared from these parasitized hosts. Furthermore, there are some biological data on other species of


204

Tetrastichinae (Eulophidae). It is known that most Tetrastichinae complete their life cycle in 15-25 days. Gumovsky et al. (2007) observed imaginal hemolymph feeding by females of B. elasmi on

larvae and pupae of Polistes dominulus and P. gallicus (Vespoidea, Vespidae). However, we did not observe hemolymph feeding by females of B. crassicornis on larvae.

Figure 1. Baryscapus crassicornis and its host Lixus nordmanni: A) adult of B. crassicornis

parasitizing the host larva, B) exit holes of the parasitoid specimens on

mummy larva; C) the parasitoid larvae in a mummy pupa, D) parasitoid exit

holes on a mummy pupa, E) exit hole and the parasitoid adult on a host adult;

F) parasitoid larvae in an adult cadaver.

A

D

B

E

C

F


205

Pronotalia carlinarum was reared as a gregarious endoparasitoid from puparia of M. heracleana (Figure 2). In total, 96 fl y puparia were obtained and

17 of them were parasitized. Th us, the parasitization rate was 17.7%. Th e wasps emerged through a single hole, mostly in the anterior part of puparia, but occasionally from posterior and rarely medial parts. P. carlinarum is a parasite of dipteran puparia, mainly Tephritidae, Calliphoridae, Chloropidae, Cecidomyiidae, and Agromyzidae (Domenichini, 1966; Graham, 1991; Vikberg, 2005; Nartshuk, 2006; Yegorenkova, 2008) and Malacosoma neustria (Lepidoptera: Lasiocampidae) (Herting, 1976). Th e only known Agromyzidae hosts of P. carlinarum are Phytomyza sp. (Tsybul’skaya et al., 1978) and Phytomyza orobanchia (Domenichini, 1966; Kostjukov, 1978). M. heracleana is a new genus and species record for this parasitoid. P. carlinarum associates mostly with plants from the Asteraceae (Graham, 1991; Öncüer, 1991; Bathon and Tirry, 2005) and Orobanchaceae (Tsybul’skaya et al., 1978). Th erefore, the parasitoid associating with Apiaceae is a new record. Each parasitoid female parasitized the host puparia for approximately 60 min. It required 12 days to complete development from egg to adult. A maximum of 25 parasitized adults (6 males and 19

females) were observed from 1 puparium. However, generally more females develop than males. When parasitized puparia were collected, only males were reared. Th e fact that 13 males, 9 males, and 6 males developed in 3 diff erent puparia suggests arrhenotoky. Clausen (1940) determined that generally about 3% of the progeny of mated females of Melittobia chalybii Ashmead are male. Although the proportion is small and was further reduced by combat, practically all females were eventually mated and the males of this species were found to be haploid, derived from unfertilized eggs of either mated or virgin females. Th is condition was generally lethal, but there was no evidence for the production of biparental males.

Th e observed mating behavior of B. crassicornis is similar to the mating behavior described for other Eulophidae (Assem, 1986; Gumovsky et al., 2007). Th e male approached the female, started forewing vibration, and touched the female’s antennae with his antennal fl agella. Later, if the male was accepted, copulation occurred. However, interesting mating behavior was observed in P. carlinarum. Males eclosed earlier than the females and stayed near the parasitized host, and courtship happened aft er the eclosion of the females. Th e male approached the female and abruptly sat on the back of the female while the female was walking. Th e male then repeatedly touched his antennal fl agellum to her mouth and the antennal fl agellum above her head, while the female walked around with the male on her back. When the male was accepted, the female stopped for a short time and copulation occurred.

Homoporus febriculosus (one female) was reared from M. heracleana as a solitary endoparasitoid. Th e wasp left the host puparium by cutting the anterior part completely (Figure 3). Sixty species of Homoporus are known, distributed in the Afrotropical, Australasian,

B

A

Figure 2. Pronotalia carlinarum and puparium of its host

Melanagromyza heracleana: A) P. carlinarum adults

leaving the host puparium from the hole on the

proximal part, B) parasitoid larvae in the host

puparium settled in plant tissue.

Figure 3. Leaving style of Homoporus febriculosus from

puparium of Melanagromyza heracleana.


206

Nearctic, Neotropical, Oriental, and Palaearctic regions (Xiao et al., 2004); they are facultative hyperparasitoids that attack a number of dipteran and hymenopteran hosts in grasses (Noyes, 1998). Th e species is a solitary (and normally primary) ectoparasite (Graham, 1969), a primary parasitoid of Mayetiola destructor Say (Cecidomyiidae) (Burks, 1979) and Lasiosina herpini (=cinctipes) (Guerin-Meneville) (Chloropidae) (Th omson, 1958; Nartshuk, 2006), a parasitoid of Hymenoptera in the families Cephidae and Eurytomidae, and a hyperparasitoid of Braconidae, Eupelmidae, and Platygastridae (Peck, 1963; Burks, 1979). Abdullah et al. (1989) reared the parasitoid from larvae of Tetramesa eximia (Giraud) (Eurytomidae). M. heracleana is a new host for H. febriculosus and a new record for Turkey. H. platytaenium is also a new record for being associated with H. febriculosus. Previously, it was recorded that H. febriculosus associates with plants from Poaceae (Peck, 1963; Abdullah et al., 1989).

Didyctium brunnea (Figure 4) was reared as a solitary endoparasitoid from puparia of L. albidipennis in stems of H. platytaenium. Th e wasp left the host by partially cutting open the puparium. Eucolidae is the largest and most widely distributed of the parasitic families in the Cynipoidea. However, there is not much knowledge of Didyctium species. D. brunnea was formerly recorded only from Sweden (Nartshuk, 2005). It is a new record for the Turkish fauna. Phoridae (Diptera) was recorded as a host for Didyctium sp. from Bermuda (Hilburn et al., 1990). It is also known that they are solitary endoparasitoids that oviposit in the larval stage of cyclorrhaphous Diptera and emerge as adults from the host puparium (Wharton et al., 1998). Th e Chloropidae family with L. albidipennis is a new host record for D. brunnea, which associates with H. platytaenium.

Within this study, the hole(s) or cutting types made by the parasitoids while leaving their hosts

were described. Some biological parameters were also given for P. carlinarum and B. crassicornis. In addition, the insects were determined as new hosts for all parasitoids and the fi rst parasitoid records for the fl ies. Chloropidae is a new record host family for D. brunnea aft er Phoridae. In addition, D. brunnea and H. febriculosus are recorded from Turkey for the fi rst time.

Acknowledgments

Th e authors are grateful to Mattias Forshage of the Department of Systematic Zoology, Uppsala University, Sweden, for identifi cation of eucolid specimens and to Zoya Yefremova and Ekaterina Yegorenkova of the Department of Zoology, Ulyanovsk State Pedagogical University, Ulyanovsk, Russia, for identifi cation of eulophids.

A

B

C

Figure 4. Parasitoid Didyctium brunnea and its host Lasiambia

albidipennis: A) exit style of L. albidipennis from its

puparium, B) parasitoid in the host puparium, C) exit

style of the parasitoid from the host puparium.

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