Microsoft Word - 0602_Stankovic_et_al BIOLOGICA NYSSANA 1 (1-2) December 2010: 117-122 Stanković S. et al. Betula species as host plants for various insects… 117 Original Article ! Betula species as host plants for various insects parasitized by braconids (Hymenoptera: Braconidae) in Serbia Saša Stanković*, Vladimir Žikić, Marijana Ilić University of Niš, Faculty of Science and Mathematics, Department of Biology and Ecology, Višegradska 33, 18000 Niš, Serbia E-mail: sasasta@gmail.com Abstract: Stanković, S., Žikić, V., Ilić, M.: Betula species as host plants for various insects parasitized by braconids (Hymenoptera: Braconidae) in Serbia. Biologica Nyssana, 1 (1-2), December 2010: 117-122. This work presents braconid wasps which can be found on insects attacking birches, especially Betula alba and B. pubescens (Betulaceae) which are autochthonous in Serbia. We have found 49 braconid species from 26 genera on 40 phytophagous insects; one from the hemimetabolous order: Homoptera: Homoptera and three from the holometabolous orders: Coleoptera, Hymenoptera and Lepidoptera. Registered braconid species belong to the subfamilies: Aphidiinae, Braconinae, Doryctinae, Euphorinae, Exothecinae, Microgastrinae, Orgilinae, Rhysipolinae and Rogadinae. Although most of the registered phytophagous insects pose a significant threat to Betula species, the two species: Epirrita autumnata (Geometridae) and Lymantria dispar (Noctuidae) are the most important, because they can defoliate entire forests when their populations are in gradation. Also, there are two buprestid pests Agrilus anxius native to North America and A. planipennis (Buprestidae) from Central Asia which are considered as potentially invasive species. Key words: Betula, Braconidae, hosts, tritrophic associations, Serbia Introduction ! Braconidae wasps comprise at least 50.000 species of solitary or gregarious ecto- and endoparasitoids that parasitize larvae of their hosts, as well as eggs and very rarely recorded, the adult stage. The body size of braconid wasps is in range from 0.5 mm to over 20 cm including the “fake ovipositor” (S t a r ý , 1970, 1988; S h a w & H u d d l e s t o n , 1991). There are two strategies among Braconidae wasps: idiobionts that permanently parasitize their host before laying eggs and konobionts that allow the host to continue developing while the larvae feed within the host’s body. The great majority of Braconidae are cosmopolitan and polyphagous insects. Some species show different degrees of host specificity. There are programs of utilization of braconid wasps and other insects as biological control agents starting from B a i r d (1958), M a t h e w s (1974), L e w i s et al. (1977, 1990), over the fieldworks such as biocontrol of olive fruit flies (S i m e et al., 2006; Y o k o y a m a et al., 2008), to brand-new, K u l a et al. (2010). Not much data exists about the insect pests feeding on birch and their parasitoids from the family Braconidae in Europe, especially in Serbia. Some sporadically records exist in the following journals: (T o m a n o v i ć & K a v a l l i e r a t o s , 2002; K a v a l l i e r a t o s et al., 2002, 2004). World fauna of Braconidae which attack pests in the birch communities is poorly investigated as well. Birches are autochthones for the greater part of Europe, as well as for the territory of Serbia. We have chosen to present this work in this journal because the first issue is dedicated to Vlasina Lake, which is the place full of native birches: Betula alba and B. pubescens (Betulaceae). Most important parasitoids 10th SFSES • 17-20 June 2010, Vlasina lake1 (1-2) • December 2010: 117-122 BIOLOGICA NYSSANA 1 (1-2) December 2010: 117-122 Stanković S. et al. Betula species as host plants for various insects… 118 in biological control of the species from the genus Agrilus (Coleoptera: Buprestidae), could be Spathius agrili Yang 2005, (Braconidae) found in the USA on European birch Betula alba (Yang et al. 2008). The host range of S. agrili is presented by 18 wood boring insects belonging to the genus Agrilus, who are present on the other host plants such as Fraxinus, Prunus and Alianthus. Material and methods The examined parasitoid wasps for this study were collected from the hosts feeding on Betula alba and B. pubescens all over Serbia. In the tritrophic associations: parasitoid-host-plant include all hosts found in Europe. One part of specimens is deposited at the Faculty of Sciences and Marthematics, Department of Biology and Ecology, University of Niš, Serbia while the rest of specimens are at the Faculty of Biology, University of Belgrade, Serbia. Identification of birch species was done according to V u k i ć e v i ć (1970). Results and discussion The parasitoid subfamilies, genera and species and their hosts are arranged in four tables as trophic associations connected by (X). The total number of 49 braconids species from 26 genera belong to the following subfamilies: Aphidiinae, Braconinae, Doryctinae, Euphorinae, Exothecinae, Microgastrinae, Orgilinae, Rhysipolinae and Rogadinae. We have found 42 host species belonging to four insect orders: Coleoptera, Homoptera, Hymenoptera and Lepidoptera (Tab. 1). All registered host species are phytophagous insects feeding on leaves or they are xylophagous on birches. The trophic relations between Aphidiinae and aphid hosts (Homoptera: Aphididae) are presented in the table 2. The species Callaphis flava (Aphididae) is registered as the host of four Aphidiinae wasps: Aphidius aquilus Mackauer, 1961, Praon flavinode (Haliday, 1833), Trioxys betulae (Marshall, 1896) and T. cirsii (Curtis, 1831). Parasitoid wasp Aphidius aquilus attack three of four recorded aphids. The ectoparasitoid groups of Braconidae witch parasitize coleopteran and hymenopteran host larvae are shown in the table 3. The subfamily Braconinae is presented by five parasitoids of Coleoptra species coming from Curculionidae and Cerambycidae. Bracon obscurator Nees 1811 was found as parasitoid of the genus Trypodendron: T. domesticum and T. signatum (Curculionidae). For buprestid Chrysobothris affinis (Buprestidae) we noted four natural enemies: Glyptomorpha pectoralis (Brullé 1832), Pseudovipio castrator (Fabricius 1798), Vipio appellator (Nees 1834) from the subfamily Braconinae and Doryctes leucogaster (Nees 1834) from the subfamily Doryctinae. The species Iphiaulax impostor (Scopoli 1763) parasitizes Aegomorphus clavipes and Leiopus nebulosus from the family of lonhorned beetles (Cerambycidae). Braconidae attacking the caterpillars of various lepidopteran families found on birches belong to the genus Bracon are B. abbreviator Nees 1834, B. discoideus Wesmael 1838, B. hebetor Say 1836, B. intercessor Nees 1834, B. romani Fahringer 1927 and B. variegator Spinola 1808 (Tab. 4). Among Bracon species the most important is polyphagous B. intercessor which attacks various insects from coleopteran families, especially Curculionidae and Lepidoptera, Sessidae - Synanthedon culiciformis, Paranthrene tabaniformis. Another important species is Bracon hebetor recorded from many larvae of Crambidae, Gelechiidae, Noctuidae and Tortricidae (Milonas, 2005); an important natural enemy of Indian meal moth Plodia interpunctella, (Pyralidae), common as pest of stored products. Subfamily Doryctinae is presented by six species from four genera attacking different hosts form the order Coleoptera: Dendrosoter protuberans (Nees 1834), Doryctes leucogaster (Nees 1834), Ontsira ignea (Ratzeburg 1852), O. imperator (Haliday 1836), Spathius curvicaudis Ratzeburg 1844 and S. rubidus (Rossi 1794), Tab. 3, and from Lepidoptera, only one but the most important and extremely polyphagous species, Lymantiria dispar from the family Noctuidae. It is interesting that the presence of any Spathius parasitoid of Agrylus cynaescens –species group (Buprestidae), native in Europe, but an invasive alien pest in North America is not reported in Europe (J e n d e k & G r e b e n n i k o v , 2009). One of the candidates for the biological control of A. cynaescens is Spathius rubidus known as polyphagous on various coleopteran families: Buprestidae, Cerambycidae, Curculionidae, and Rhizophagidae as well as Xiphydriidae from the order of Hymenoptera. In addition to this species, we report it as parasitoid of two species of Agrylus: A. angustulus and A. hastulifer (Buprestidae) and Leiopus nebulosus and Rhagium mordax from the family of Cerambycidae. Diversity and some parasitoid-host data are the best known for this subfamily among ectoparasitic (B e l o k o b y l s k i j & Ž i k i ć , 2009). From the ectoparasitoid subfamily Exothecinae we registered only two species: Colastes braconius Haliday 1833 parasitizes on Heterarthrus vagans sawfly (Tenthredinidae) and on another extremely polyphagous species Epirrita autumnata Geometridae), BIOLOGICA NYSSANA 1 (1-2) December 2010: 117-122 Stanković S. et al. Betula species as host plants for various insects… 119 Table 1. The list of pests on Betula alba and B. pubescens Order Family Species Homoptera Aphididae Callaphis flava Mordvilko, 1928 Euceraphis betulae (Koch 1855). Euceraphis punctipennis (Zetterstedt 1828) Symydobius oblongus (von Heyden, 1837). Coleoptera Buprestidae Agrilus angustulus (Illiger 1803) Agrilus cyanescens Ratzeburg 1837 Agrilus hastulifer Ratzeburg 1837 Chrysobothris affinis (Fabricius 1794) Dicerca berolinensis (Herbst 1779) Curculionidae Scolytus ratzeburgi Janson 1856 Trypodendron domesticum (Linnaeus 1758) Trypodendron signatum (Fabricius, 1787) Cerambycidae Aegomorphus clavipes (Schrank 1781) Leiopus nebulosus (Linnaeus 1758) Rhagium mordax (De Geer 1775) Hymenoptera Tenthredinidae Fenusa pumila Leach 1817 Fenusella nana (Klug 1816) Heterarthrus vagans (Fallen 1808) Scolioneura betuleti (Klug 1816) Xiphydriidae Xiphydria prolongata (Geoffroy 1785) Lepidoptera Geometridae Cyclophora pendularia (Clerck 1759) Epirrita autumnata (Borkhausen 1794) Hypagyrtis unipunctata (Haworth 1809) Gracillariidae Caloptilia betulicola (Hering 1928) Heliozelidae Heliozela betulae Stainton 1890 Noctuidae Euproctis chrysorrhoea (Linnaeus 1758) Hyphantria cunea (Drury 1773) Lymantria dispar (Linnaeus 1758) Orthosia gothica (Linnaeus 1758) Orthosia incerta (Hufnagel 1766) Lasiocampidae Malacosoma neustria (Linnaeus 1758) Psychidae Megalophanes viciella (Denis & Schiffermuller 1775) Sesiidae Synanthedon culiciformis (Linnaeus 1758) Tortricidae Acleris hastiana (Linnaeus 1758) Adoxophyes orana Fischer von Rösslerstamm 1834) Apotomis sororculana (Zetterstedt 1839) Archips rosana (Linnaeus 1758) Pandemis cerasana (Hubner 1786) Pandemis heparana (Denis & Schiffermuller 1775) Geometridae Cyclophora pendularia (Clerck 1759) Hypagyrtis unipunctata (Haworth 1809) Coleophoridae Coleophora serratella (Linnaeus 1761) and Shawiana catenator (Haliday 1836) on caterpillars of Caloptilia betulicola (Gracillariidae). Subfamily Rogadinae assembles eight species of Aleiodes: A. circumscriptus (Nees 1834), A. gastritor (Thunberg 1822), A. nigricornis Wesmael 1838, A. pallidator (Thunberg 1822), A. rossicus (Kokujev 1898) and A. sanctihyacinthi (Provancher 1880), distributed mostly in whole Europe (Aydogdu & Beyarslan, 2006) and Petalodes compressor (Herrich-Schäffer 1838). The species A. pallidator has been recorded as parasitoid of four lepidopteran larvae: Cyclophora pendularia (Geo- Table 2. Subfamily Aphidiinae and the aphid hosts C al la ph is fla va E uc er ap hi s be tu la e E uc er ap hi s pu nc tip en ni s S ym yd ob iu s ob lo ng us Aphidius aquilus X X X Betuloxys compressicornis X X Praon flavinode X Trioxys betulae X X Trioxys cirsii X BIOLOGICA NYSSANA 1 (1-2) December 2010: 117-122 Stanković S. et al. Betula species as host plants for various insects… 120 metridae), Lymantria dispar, Megalophanes viciella (Psychidae) and Apotomis sororculana (Tortricidae) (Tab. 4). The last registreted ectoparasitic Braconidae subfamily is Rhysipolinae, with only one species, Rhysipolis meditator (Haliday 1836) on Caloptilia betulicola (Gracillariidae). Table 3. Subfamilies of ectoparasitoid Braconidae on coleopteran and hymenopteran hosts. T ry po de nd ro n do m es tic um T ry po de nd ro n si gn at um S co ly tu s ra tz eb ur gi A gr ilu s cy an es ce ns A gr ilu s an gu st ul us A gr ilu s ha st ul ife r C hr ys ob ot hr is a ffi ni s D ic er ca b er ol in en si s A eg om or ph us c la vi pe s Le io pu s ne bu lo su s R ha gi um m or da x F en us a pu m ila F en us el la n an a H et er ar th ru s va ga ns S co lio ne ur a be tu le ti X ip hy dr ia p ro lo ng at a Braconinae Bracon obscurator X X Glyptomorpha pectoralis X Iphiaulax impostor X X Pseudovipio castrator X Vipio appellator X Doryctinae Dendrosoter protuberans X X Doryctes leucogaster X Ontsira ignea X Ontsira imperator X X Spathius curvicaudis X Spathius rubidus X X X X X Exothecinae Colastes braconius X Shawiana catenator X X X X Table 4. Subfamilies of ectoparasitoid Braconidae on lepidopteran hosts C yc lo ph or a pe nd ul ar ia H yp ag yr tis u ni pu nc ta ta C al io ph ili a be tu lic ol a H el io ze la b et ul ae E pi rr ita a ut um na ta Ly m an tr ia d is pa r E up ro ct is s im ili s H yp ha nt ria c un ea O rt ho si a go th ic a O rt ho si a in ce rt a M al ac os om a ne us tr ia M eg al op ha ne s vi ci el la S yn an th ed on c ul ic ifo rm is A cl er is h as tia na A do xo ph ye s or an a A po to m is s or or cu la na A rc hi ps r os an a P an de m is c er as an a P an de m is h ep ar an a Braconinae Bracon abbreviator X Bracon discoideus X Bracon hebetor X Bracon intercessor X Bracon romani X Bracon variegator X X Doryctinae Doryctes leucogaster X Exothecinae Colastes braconius X Rogadinae Aleiodes circumscriptus X Aleiodes gastritor X X Aleiodes nigricornis X X Aleiodes pallidator X X X X Aleiodes rossicus X X X Aleiodes sanctihyacinthi X Aleiodes signatus X Aleiodes testaceus, X Petalodes compressor X Rhysipolinae Rhysipolis meditator X BIOLOGICA NYSSANA 1 (1-2) December 2010: 117-122 Stanković S. et al. Betula species as host plants for various insects… 121 In this study we have found the data of three endoparasitic braconid subfamilies: Euphorinae, Microgastrinae and Orgilinae (Tab. 5). As Bracon obscurator, Cosmophorus regius Niezabitowski 1910 (Euphorinae) shows the same affinity to the species of Trypodendron (Tab. 2). Two species of Meteorus, M. pulchricornis (Wesmael 1835) and M. meteorus, M. pulchricornis (Wesmael 1835) and M. versicolor (Wesmael 1835) attack the most common pest Lymantria dispar. Polyphagous Epirrita autumnata is the host of solitary endoparasitoid Zele deceptor (Wesmael 1835). Mostly gregarious, Microgastrinae are presented by nine members on Betula spesies that eight of them attack Lymantria dispar: three species of Apanteles: A. lacteicolor Viereck 1911, A. melanoscelus (Ratzeburg 1844) and A. xanthostigma (Haliday 1834), one species of Cotesia: C. lomerata (Linnaeus 1758), Microgaster hospes Marshall 1885, and three species of Protapanteles: P. fulvipes (Haliday 1834), P. liparidis (Bouche 1834) and P. immunis (Haliday 1834). Larvae of Epirrita autumnata is parasitized by Cotesia jucunda (Marshall 1885). There is only one species of Orgilinae, Orgilus punctulator (Nees 1811) has been found as pest of Coleophora serratella (Coleophoridae). Table 5. Subfamilies of Euphorinae, Microgastrinae and Orgilinae and their hosts. Tr yp od en dr on d om es tic um Tr yp od en dr on s ig na tu m E pi rri ta a ut um na ta Ly m an tri a di sp ar C ol eo ph or a se rra te lla Euphorinae Cosmophorus regius X X Meteorus pulchricornis X Meteorus versicolor X Zele deceptor X Microgastrinae Apanteles lacteicolor X Apanteles melanoscelus X Apanteles xanthostigma X Cotesia glomerata X Cotesia jucunda X Microgaster hospes X Protapanteles fulvipes X Protapanteles liparidis X Protapanteles immunis X Orgilinae Orgilus punctulator X Conclusion We noted that pest insects make no difference on which Betula species they feed. The most important pests on Betula as well as other trees are polyphagous species Lymantria dispar and Epirrita autumnata, because they can defoliate entire forests when their populations are in gradation. We have found that larvae of Lymantria dispar on birches are attacked by 11 parasitoid species from the subfamilies Braconinae, Rogadinae, Euphorinae and Microgastrinae. The moth Epirrita autumnata can be very dangerous in birch forests. The example from northern Sweden shows that this pest’s caterpillars can defoliate birch forests, causing death of stems of the polycormic trees as a result (T e n o w , et al., 2004). There are three buprestid pests of the genus Agrilus found on Betula alba and B. pubescens: A. angustulus, A. cyanescens, A. hastulifer. They are extremely polyphagous wood borers. For now there is no data of the natural enemies of A. cyanescens. Agrilus anxius, which is native to North America and A. planipennis from Central Asia are considered as potentially invasive species. Acknowledgements. The authors wish to express their sincere thankfulness to Dr. Ž. Tomanović (Faculty of Biology, Belgrade, Serbia). For the present work the authors were supported by the Ministry of Science and Environment Protection of the Republic of Serbia (Grant No. 143006B). References Aydogdu, M., Beyarslan, A. 2006: First records of Aleiodes Wesmael, 1838 species in East Marmara Region of Turkey (Hymenoptera: Braconidae: Rogadinae). Acta Entomologica Slovenica, 14(1): 81–88 Baird, A. B. 1958: Biological control of insects and plant pests in Canada. Prc 10th Int. Cong. Ent. 4: 483-485. Belokobylskij, S. A., Žikić, V., 2009: New data on cyclostome braconid subfamilies Doryctinae, Exothecinae, Rogadinae and Braconinae (Braconidae: Hymenoptera) of Serbia and neighbouring territories. Acta Entomologica Serbica. 14(1): 65-71 Georgiev, G. 2005: Bioecological characteristics of Bracon intercessor Nees (Hymenoptera: Braconidae) as a parasitoid of the poplar clearwing moth, Paranthrene tabaniformis (Rott.) (Lepidoptera: Sesiidae) in Bulgaria. Journal of Pest Science, 78: 161-165 BIOLOGICA NYSSANA 1 (1-2) December 2010: 117-122 Stanković S. et al. Betula species as host plants for various insects… 122 Jendek, J., Grebennikov, V. V. 2009: Revision of the Agrilus cyanescens species-group (Coleoptera: Buprestidae) with description of three new species from the east Palaearctic region. Zootaxa, 2139: 43–60. Kavallieratos, N.G., Athanassiou, C., Stathas, G., Tomanović Ž. 2002: Aphid parasitoids (Hymenoptera, Braconidae) on citrus: seasonal abundance, association with the species of host plant and sampling indices. Phytoparasitica, 30: 365-377. Kavallieratos, N. G., Tomanović, Ž., Starý, P., Athanassiou, C. G., Sarlis, G. P., Petrović, O., Niketić, M. A., Anagnou-Veroniki, M., 2004: A survey of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) of Southeastern Europe and their aphid-plant associations. Appl. Entomol. Zool. 39 (3): 527–563. Kula, R. R., Boughton, A.J., Pemberton, R.W., 2010: Stantonia pallida (Ashmead) (Hymenoptera: Braconidae) Reared from Neomusotima conspurcatalis Warren (Lepidoptera: Crambidae), a Classical Biological Control Agent of Lygodium microphyllum (Cav.) R. Br. (Polypodiales: Lygodiaceae). Proceedings of the Entomological Society of Washington, 112(1): 61-68. Lewis, W.J., Nordlund, D.A., Gross, H.R., Jr., Jones, R.L., Jones, S.L., 1977: Kairomones and their use for management of entomophagous insects: V. Moth scales as a stimulus for predation of Heliothis zea (Boddie) eggs by Chrysopa carnea Stephens larvae. J. Chem. Ecol. 3: 483-487. Lewis, W.J., Vet, L.E.M., Tumlinson, J.H., van Lenteren, J.C., Papaj, D.R., 1990: Variations in parasitoid foraging behavior: essential element of a sound biological control theory. Environmental Entomology 19: 1183-1193. Mathews, R.W., 1974: Biology of Braconidae. Annual Review of Entomology 19: 15-32. Milonas, P.G., 2005: Influence of initial egg density and host size on the development of the gregarious parasitoid Bracon hebetor on three different host species. Biocontrol, 50: 415-428. Shaw, M.R., Huddleston, T., 1991: Classification and biology of braconid wasps (Hymenoptera: Braconidae). Royal Entomological Society of London 7, 11: 1-126. Sime, K.R., Daane, K.M., Nadel, H., Funk, C.S., Messing, R.H., Andrews Jr, J.W., Johnson, M.W., Pickett, C.H., 2006: Diachasmimorpha longicaudata and D. kraussii (Hymenoptera: Braconidae), potential parasitoids of the olive fruit fly. Biocontrol Science and Technology, 16(2): 169-179. Starý, P., 1988: Aphidiidae. Aphids, Their Biology, Natural Enemies and Control. Vol. 2B (A. K. Minks and P. Harrewijn eds.). Elsevier, Amsterdam, 171–184 pp. Starý, P., 1970: Biology of Aphid Parasites (Hymenoptera:Aphidiidae). Dr W. Junk, The Hague, 643 p. Tomanović, Ž., Kavallieratos, N.G., 2002: Trioxys Haliday (Hymenoptera: Braconidae: Aphidiinae) in Serbia and Montenegro. Acta Entomologica Serbica, 7(1/2): 67-81 Vukićević, E., 1970: Rod Betula L. In: Josifović, M., ed.: Flora SR Srbije, 2. SANU, Beograd. Yang. Z-Q., Wang, X-Y., Gould, J.R., Wu, H., 2008: Host specificity of Spathius agrili Yang (Hymenoptera: Braconidae), an important parasitoid of the emerald ash borer. Biological Control, 47: 216–221. Yokoyama, V.Y., Rendo, P.A., Sivinski, J., 2008: Psyttalia cf. concolor (Hymenoptera: Braconidae) for biological control of olive fruit fly (Diptera: Tephritidae) in California. Environ. Entomol. 37(3): 764-773. Tenow, O., Bylund, H., Karlsson, P. S., Hoogesteger, J., 2004: Rejuvenation of a mountain birch forest by an Epirrita autumnata (Lepidoptera: Geometridae) outbreak. Acta Oecologica, 25(1/2): 43-52.