E. KOÇAK, M. ÖZDEMİR

Turk J Zool 2012; 36(2): 201-208 © TÜBİTAK Research Article doi:10.3906/zoo-1008-129

Parasitic reared from the 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 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) () and Homoporus febriculosus (Girault) () 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

* E-mail: [email protected]

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

(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

Introduction and rare species recorded form Croatia, France, Italia, Th e genus Heracleum L. (Apiaceae) includes southern Russia, and the Czech Republic (Kubik, approximately 125 species worldwide and 23 in 2006) and Turkey (Koçak et al., 2009). Th is species Turkey (Pimenov and Leonov, 2004). Heracleum is known as saprophagous (Nartshuk, 2005) and its platytaenium Boiss. is a perennial herbaceous and larvae are generally found near or on decomposed monocarpic endemic species belonging to the stems, caused by some larvae of L. nordmanni and Euxine phytogeographic region (Davis, 1972) and M. heracleana. Moreover, the larvae feed inside the it yields furanocoumarins (Nielsen, 1970), which dead bodies of L. nordmanni larvae or pupae (Koçak are known to be insect repellents and suppress the et al., 2009). growth of some insect species (Berenbaum, 1981; Melanagromyza Hendel is among the largest Moore and Debboun, 2006). So far, many studies genera of the family Agromyzidae, representing have been carried out on the insects of Heracleum 357 species in the world fauna. Th eir primary species in the world, especially on their biology and feeding habit is internal stem-boring in Apiaceae. natural enemies (Burki and Nentwig, 1997; Hansen M. heracleana was recorded as stem-borers in et al., 2006; Hattendorf et al., 2006; Page et al., 2006; Heracleum mantegazzianum Sommier & Levier in Koçak et al., 2009). In this study, the parasitoids were Russia (Zlobin, 2005) and H. platytaenium in Turkey inspected on Lixus nordmanni Hochhuth (Coleoptera: (Koçak et al., 2009). Curculionidae), Melanagromyza heracleana Zlobin Although there are some records of parasitoids (Diptera: Agromyzidae), and Lasiambia albidipennis of some species of the genera Lasiambia and (Strobl) (Diptera: Chloropidae) from the stems and Melanagromyza, there are no parasitoid records on L. branches of H. platytaenium. albidipennis or M. heracleana. As for the host insects, the genus Lixus is wildly In the present paper, we report on new faunistic distributed worldwide and comprises over 500 studies, biological data on parasitoids, and host- species, with over 150 species in the Palaearctic region parasitoid relationships. (Csiki, 1934; Ter-Minassian, 1967). L. nordmanni is distributed in the Caucasus (Petri, 1904/1905) and Turkey (Gültekin, 2006; Koçak et al., 2009). Materials and methods Th is species feeds on Heracleum species (Gültekin, Heracleum platytaenium specimens were collected 2006). Some Lixus species are actual agricultural in the vicinity of Kızılcahamam (between 40°33ʹN pests (Nikulina, 1989; Volovnik, 1994), and some and 40°30ʹN and 32°33ʹE and 32°38ʹE, approximately can potentially be used for biological control of 1000 m a.s.l.), in Ankara Province in July-September weeds (Gültekin, 2004). Chlorocytus longicauda (Th .) 2008. Plants including the diff erent stages of insects (Hymenoptera: Pteromalidae) was reared from the were collected. In the insectariums, the stems were pupal stage of Lixus nordmanni by Gültekin (2006). investigated and kept separate from the umbels Th e Lasiambia Sabrosky genus consists of 12 (seeds and fl ower stalks) in diff erent cabins. Th e species in Europe. L. albidipennis is a little-known diff erent insect species were separated individually

202 E. KOÇAK, M. ÖZDEMİR

into diff erent developmental stages in small cut the weevil L. nordmanni and fl y M. heracleana, stem parts. Parasitization rates were also determined respectively. Gibson (1993) found that according to the number of parasitized individuals species were mostly internal primary parasitoids of the among all individuals brought in from the fi eld. eggs, larvae, or pupae of Lepidoptera, Coleoptera, and Biological studies were carried out for P. Diptera, but they have been reared from members of carlinarum on puparia of M. heracleana and for B. 10 insect orders, and a few species are phytophagous, crassicornis on larva of L. nordmanni at 25 ± 1 °C and predaceous on gall mites (Acari), or parasitoids 70 ± 5% RH with a photoperiod of 16:8 (L:D) in a of thrips larvae (Th ysanoptera). Tetrastichines are climate chamber. Th e parasitoid adults were fed with equally diverse in other aspects of their biology, such honey. In total, 4 host insect specimens were used for that few generalizations can be made about the group parasitization separately for both parasitoids. In July, as a whole. Species can be solitary or gregarious, the fourth stages of Lixus larvae collected on plant primary or secondary parasitoids, and monophagous stems were separated and observed for 3 days to be to polyphagous. Although they predominantly attack sure they were not parasitized by any parasitoid. larvae or pupae, many egg parasitoids are known, Similar observations for both parasitization and and a few are even parasitoids of adults (LaSalle and development of adult fl ies were conducted during Boler, 1994). 1 week for overwintering M. heracleana puparia Lixus nordmanni is a newly recorded host for B. collected at the end of September. General mating crassicornis (Figure 1). Th e parasitoid was reared behavior of the parasitoids in petri dishes was as an endoparasitoid from larvae of various stages, observed and easily noted with the naked eye. Th ree pupae, and adult stages of L. nordmanni. Diff erent repetitions with 3 diff erent couples of parasitoids stages of L. nordmanni (72 adults, 41 pupae, and 35 were done on the same day for each parasitoid species larvae) were obtained and their parasitization rates under laboratory conditions. were determined to be 15.2%, 14.6%, and 28.5%, A pteromalid specimen was identifi ed using the respectively, with an average parasitization of 18.9%. identifi cation key of Dzhanokmen (1987). Th e adult emerge through a few circular holes from diff erent parts of the body. H. platytaenium is All specimens used in this study were deposited a new host plant for this parasitoid. B. crassicornis at the Plant Protection Central Research Institute in was described from Asteraceae on Larinus species Ankara, Turkey, except for 2 males and 2 females of (Coleoptera: Curculionidae) (Domenichini, 1966; D. brunnea that are at the Department of Systematic Graham, 1991) and Tephritis conycifoliae (Diptera: Zoology, Uppsala University, Sweden. Tephritidae) (Vidal, 1997). Yegorenkova (2008) recorded B. endophiticus (Dominichini) from Results and discussion Lixus iridis Olivier (Coleoptera: Curculionidae) on Satureja hortensis (Labiatae). Doganlar (1993) In the current study, parasitic wasps and their determined the parasitoid from Onopordon sp. hosts on H. platytaenium were determined to be (Asteraceae) as the fi rst record in Turkey. Recently, Didyctium brunnea (Belizin) (Eucolidae) from L. a pteromalid parasitoid, C. longicauda, was reared albidipennis, Pronotalia carlinarum (Szelenyi & from L. nordmanni on Heracleum sp. in Turkey Erdos) (Eulophidae) and Homoporus febriculosus (Gültekin, 2006). In the present study, B. crassicornis (Girault) (Pteromalidae) from M. heracleana, and females paralyzed the L. nordmanni larva and later Baryscapus crassicornis (Erdos) (Eulophidae) from oviposited into the larvae over the course of 20-30 L. nordmanni. None of the parasitoids of the fl ies M. min. It is an idiobiont parasitoid that paralyzes the heracleana and L. albidipennis were known on these host permanently. It required 19-20 days to complete hosts. Previously, a pteromalid pupal parasitoid (C. development from egg to adult. A maximum of 52 longicauda) of L. nordmanni was described from specimens (9 males and 43 females) and a minimum Turkey (Gültekin, 2006). of 18 specimens (3 males and 15 females) were Two eulophid species, B. crassicornis and P. reared from these parasitized hosts. Furthermore, carlinarum from Tetrastichinae, were reared from there are some biological data on other species of

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

A B C

D E F

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.

Tetrastichinae (Eulophidae). It is known that most larvae and pupae of Polistes dominulus and P. gallicus Tetrastichinae complete their life cycle in 15-25 (Vespoidea, Vespidae). However, we did not observe days. Gumovsky et al. (2007) observed imaginal hemolymph feeding by females of B. crassicornis on hemolymph feeding by females of B. elasmi on larvae.

204 E. KOÇAK, M. ÖZDEMİR

Pronotalia carlinarum was reared as a gregarious females) were observed from 1 puparium. However, endoparasitoid from puparia of M. heracleana generally more females develop than males. When (Figure 2). In total, 96 fl y puparia were obtained and 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 A 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). B Th e male approached the female, started forewing vibration, and touched the female’s antennae with Figure 2. Pronotalia carlinarum and puparium of its host his antennal fl agella. Later, if the male was accepted, Melanagromyza heracleana: A) P. carlinarum adults copulation occurred. However, interesting mating leaving the host puparium from the hole on the behavior was observed in P. carlinarum. Males proximal part, B) parasitoid larvae in the host eclosed earlier than the females and stayed near the puparium settled in plant tissue. parasitized host, and courtship happened aft er the eclosion of the females. Th e male approached the 17 of them were parasitized. Th us, the parasitization female and abruptly sat on the back of the female while rate was 17.7%. Th e wasps emerged through a the female was walking. Th e male then repeatedly single hole, mostly in the anterior part of puparia, touched his antennal fl agellum to her mouth and the but occasionally from posterior and rarely medial antennal fl agellum above her head, while the female parts. P. carlinarum is a parasite of dipteran puparia, walked around with the male on her back. When the mainly Tephritidae, Calliphoridae, Chloropidae, male was accepted, the female stopped for a short Cecidomyiidae, and Agromyzidae (Domenichini, time and copulation occurred. 1966; Graham, 1991; Vikberg, 2005; Nartshuk, 2006; Yegorenkova, 2008) and Malacosoma neustria Homoporus febriculosus (one female) was reared (Lepidoptera: Lasiocampidae) (Herting, 1976). Th e from M. heracleana as a solitary endoparasitoid. Th e only known Agromyzidae hosts of P. carlinarum left the host puparium by cutting the anterior part are Phytomyza sp. (Tsybul’skaya et al., 1978) and completely (Figure 3). Sixty species of Homoporus are Phytomyza orobanchia (Domenichini, 1966; known, distributed in the Afrotropical, Australasian, 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. Figure 3. Leaving style of Homoporus febriculosus from A maximum of 25 parasitized adults (6 males and 19 puparium of Melanagromyza heracleana.

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

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) A 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 B 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 C for H. febriculosus and a new record for Turkey. H. platytaenium is also a new record for being associated Figure 4. Parasitoid Didyctium brunnea and its host Lasiambia with H. febriculosus. Previously, it was recorded that albidipennis: A) exit style of L. albidipennis from its puparium, B) parasitoid in the host puparium, C) exit H. febriculosus associates with plants from Poaceae style of the parasitoid from the host puparium. (Peck, 1963; Abdullah et al., 1989). Didyctium brunnea (Figure 4) was reared as a solitary endoparasitoid from puparia of L. were described. Some biological parameters were albidipennis in stems of H. platytaenium. Th e wasp also given for P. carlinarum and B. crassicornis. In left the host by partially cutting open the puparium. addition, the insects were determined as new hosts Eucolidae is the largest and most widely distributed for all parasitoids and the fi rst parasitoid records for of the parasitic families in the Cynipoidea. However, the fl ies. Chloropidae is a new record host family for there is not much knowledge of Didyctium species. D. brunnea aft er Phoridae. In addition, D. brunnea D. brunnea was formerly recorded only from Sweden and H. febriculosus are recorded from Turkey for the (Nartshuk, 2005). It is a new record for the Turkish fi rst time. 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 Acknowledgments that oviposit in the larval stage of cyclorrhaphous Th e authors are grateful to Mattias Forshage of Diptera and emerge as adults from the host puparium the Department of Systematic Zoology, Uppsala (Wharton et al., 1998). Th e Chloropidae family with University, Sweden, for identifi cation of eucolid L. albidipennis is a new host record for D. brunnea, specimens and to Zoya Yefremova and Ekaterina which associates with H. platytaenium. Yegorenkova of the Department of Zoology, Within this study, the hole(s) or cutting types Ulyanovsk State Pedagogical University, Ulyanovsk, made by the parasitoids while leaving their hosts Russia, for identifi cation of eulophids.

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