Potential biological control agents of field bindweed, common teasel and field dodder from Slovakia

P. Tóth,1 M. Tóthova2 and L. Cagáň1

Summary Field explorations during 2001 to 2006 in Slovakia resulted in the discovery of several potential bio- logical control agents of the three weeds, field bindweed, Convolvulus arvensis L.; common teasel, fullonum L.; and field dodder, Cuscuta campestris Yuncker. The five top candidates are described in the following. The larvae of the agromyzid fly Melanagromyza albocilia Hendel (Agro- myzidae) mine in the stems and root crowns of field bindweed, causing the death of infested shoots. The number of infested plants ranged from 46.7% to 99.2% and the number of infested stems from 4.1% to 37.2% in southwest Slovakia. The larvae and adults of the tortoise beetle, Hypocassida sub- ferruginea (Schrank) (Chrysomelidae), almost completely destroyed leaves of field bindweed in some uncultivated habitats in the warmest localities of Slovakia. Development of the is rapid under favourable conditions and takes only 22 to 27 days; females have a high fecundity, and it is easy to rear. The most important natural enemy of H. subferruginea recorded in Slovakia was the egg parasit- oid Brachista pungens (Mayr) (Trichogrammatidae). Adult of gentianaeana (Hüb- ner) and roseana (Haworth) () were reared in high numbers from flowerheads of common teasel during the study. Of E. gentianaeana, only one larva was found per flowerhead, feeding within the central cavity, while larvae of C. roseana were gregarious. Especially C. roseana was destroying a large number of seeds within the flowerheads of teasel. Considerable parasitization of E. gentianaeana by Glypta mensurator (Fabricius) (Ichneumonidae) was noted. Weevils from the genus Smicronyx (Curculionidae) were found to be the principal natural enemies of dodders in Slova- kia. Larvae of Smicronyx spp. induce stem galls, which prevents flowering and fruiting of field dodder vines. Smicronyx jungermanniae (Reich) was the most abundant species, accounting for up to 96% of the total number of weevils (n = 877) reared from field dodder galls.

Keywords: Convolvulus, Dipsacus, Cuscuta, , candidates.

Introduction vulaceae, only a small number of them seem to have potential as biological control agents (Tóth and Cagáň, Field bindweed, Convolvulus arvensis L. (Convolvu- 2005). Of these, only Tyta luctuosa (Denis and Schif- laceae), has been described as the 12th worst weed in fermuller) (: Noctuidae) and Aceria mal- the world, the seventh most important in Europe and herbae Nuzzaci (Acari: Eriophyidae) have so far been the most important weed in European orchards. Field used in the classical biological control of bindweeds in bindweed tolerates a great range of environmental North America (Rees and Rosenthal, 1996). conditions and elevations; for more information on Common teasel, L. (Dipsacaceae), bindweed, see Tóth (2000). Although a relatively large grows mostly in non crop areas in Slovakia. River number of species has been recorded from the Convol- banks, roadsides and disturbed areas are the most com- mon habitats of teasel throughout Slovakia. Teasel is an invasive species in North America. Whereas the plant is not a problem on Slovakian agricultural land, it is 1 Slovak Agricultural University, Department of Plant Protection, considered a noxious weed locally in the USA. Teasels A. Hlinku 2, 949 76 Nitra, Slovak Republic. are invading plains, waste grounds, old fields, pastures 2 Slovak Agricultural University, Department of Sustainable Develop- and grow along edges of forests (Sforza, 2002). While ment, Mariánska 10, 949 01 Nitra, Slovak Republic. Corresponding author: P. Tóth . a large number of feed on teasels, no biological © CAB International 2008 control agent has up to now been introduced.

216 Potential biological control agents of field bindweed, common teasel and field dodder from Slovakia

Field dodder, Cuscuta campestris Yuncker (Cus- plants were evaluated for attack of Melanagromyza cutaceae), is an annual stem parasite with leafless, albocilia. thread-like, orange or yellow stems that twine over other plants. Field dodder is distributed worldwide and Common teasel has very low host specificity, attacking many different host plants simultaneously. There are five dodder spe- During 2003 to 2004, the study was extended to cies known in Slovakia, but C. campestris is the only plants from the genus Dipsacus. Several surveys were introduced species; for more information on dodder, conducted from April to June in southwest Slovakia, see Tóth and Cagáň (2001). C. campestris was intro- concentrating on flower-feeding insects. The plant was duced from North America to Europe in 1883 (Jehlík, mostly found in natural areas. To rear adult insects 1998). It is not yet possible to provide an authorita- and their parasitoids, flowerheads of D. fullonum were tive assessment of the biological control prospects for collected and placed in glass boxes with a perforated dodder. The surveys that have been made give an in- top under lab conditions (20°C, 70% RH). A total of dication of potential biological control candidates, but 200 flowerheads was collected. Emerged adults were knowledge of their host range and of the conditions identified. required for them to achieve effective suppression is incomplete (CAB, 1987). Field dodder The main objective of this study was to determine During the growing season 2001, 2003 and 2006, the most important insect guild feeding on the above- the occurrence of insects feeding on field dodder was mentioned weeds in Slovakia and to evaluate their po- observed irregularly in the agroecosystems of Slova- tential use in classical or inundative biological control kia following the natural phenology of dodders. A to- programmes. tal of 82 localities were chosen in different geographic and climatic regions throughout Slovakia. Collection Materials and methods sites were field dodder-infested croplands planted with various crops, fallow fields and roadsides. At each lo- Field bindweed cality, Cuscuta species were identified. The localities were inspected especially to record the presence of the During the growing season of 1998 to 1999, 2002 to weevils from the genus Smicronyx (Coleoptera: Cur- 2003 and 2005, three sites of field bindweed (Kamenica culionidae). At each collection site, field dodder plants nad Hronom, Čajkov, Vráble) in southwest Slovakia were inspected for the presence of stem galls and galls were checked weekly from mid-April until the begin- collected. To assess adult emergence, field-collected ning of October, following the natural phenology of the stem galls were placed in plastic tubes (8 cm diameter, plant. An additional seven locations were visited three 4.5 cm high) with perforated tops for aeration and kept times at monthly intervals. The locations were chosen in the laboratory at 20°C ± 1°C. Emerged adults were in different geographic and climatic regions. Besides, identified. opportunistic sampling was conducted at numerous lo- cations with different climates during different times of the year. Collection sites were grassy or weedy Results roadsides, fallow fields, C. arvensis-infested cropland During the study, 108 organisms were collected from and vacant town lots. At each collection site, plants field bindweed (see Tóth and Cagáň, 2005 for details), were inspected for damage. Insects were collected by seven from teasel, and six from dodder. sweeping (150 sweepings per site), or by aspirating or hand-picking them from plants. The field surveys were concentrated on the agromyzid fly, Melanagromyza Field bindweed abocilia Hendel (Diptera: Agromyzidae) and tortoise M. albocilia Hendel was the only species feeding beetles of the genus Hypocassida (Coleoptera: Chryso- within the stems and roots of field bindweed in Slova- melidae). More detailed methods are described in Tóth kia. Between 10% and 100% of field bindweed plants et al. (2005) and Tóth and Tóthova (2006). and up to 50% of the shoots were infested. The life his- Preliminary host-specificity tests were conducted tory of M. albocilia and impact on the host were de- with M. abocilia. Two economically important field scribed in detail by Tóth et al. (2005). M. albocilia was bindweed relatives in the Convolvulaceae, Ipomoea found in 91 locations of 132, confirming it is a com- batatas (L.) Lam. (sweet potato) and Ipomoea alba L. mon insect in Slovakia and closely related to its host (ornamental plant) were used in the experiments. Ten plant C. arvensis. Seven species of Hymenoptera were potted field bindweed plants were exposed together reared from pupae and larvae of M. albocilia as solitary, with ten plants of I. batatas and ten plants of I. alba at larval and pupal parasitoids belonging to four families: each of three corn fields infested by field bindweed in Aneuropria foersteri Kieffer (Diapriidae), Sphegigas- June 2002 and 2003. At the end of September, plants ter truncata Thomson Sphegigaster aculeata (Walker), exposed as well as 30 naturally growing bindweed Cyrtogaster vulgaris Walker (Pteromalidae), Macro-

217 XII International Symposium on Biological Control of Weeds neura (Eupelmus) vesicularis (Retzius) (Eupelmidae), erywhere in Slovakia. Larvae were feeding within the Chorebus cyparissa (Haliday) and Bracon picticornis central cavity of flowerheads and destroying the seeds. Wesmael (Braconidae). Parasitoids from the families On average, one larva damaged about ten seeds during Braconidae and Pteromalidae predominated, mak- each attempt to cut an exit hole. Infestation of plants ing up 96.3% of parasitoids that emerged. S. truncata, infested by C. roseana ranged from 70% to 100%. C. cyparissa and B. picticornis were the most abun- Larvae of C. roseana were found to feed gregariously dant parasitoids reared from M. albocilia, accounting (7–30 larvae per flowerhead), and destroyed the larg- for 36.3%, 35.6% and 21.8%, respectively, of the total est number of seeds. During the study, several para- number reared. Preliminary studies conducted in Slo- sitoids were recovered from flowerheads. Considerable vakia revealed that parasitoids suppressed 77% of the parasitization was only recorded for E. gentianaeana, stem miner population in the field. where Glypta mensurator (Fabricius) (Hymenoptera: During preliminary host-specificity tests, M. albo- Ichneumonidae) dominated. cilia attack was found in both wild and artificially ex- posed field bindweed plants at the three field localities Field dodder but no attack on I. batatas and I. alba. Tortoise beetles were important field bindweed de- Species from four orders were regularly found feed- foliators. Seven species were found in association with ing on dodder plants, i.e. aphids (Sternorrhyncha), bugs field bindweed in Slovakia. These were Cassida san- (Heteroptera), weevils (Coleoptera) and flies (Diptera). guinosa Suffrian, Cassida nebulosa Linnaeus, Cassida Aphids mostly consisted of Aphis fabae Scopoli (Aphi- stigmatica Suffrian, Cassida vibex Linnaeus, Cassida didae), bugs of Lygus rugulipennis Poppius (Miridae), murraea Linnaeus, Cassida viridis Linnaeus and Hypo- and the diptera were dominated by the stem-mining cassida subferruginea (Schrank) (Coleoptera: Chryso- fly, Melanagromyza cuscutae Hering (Agromyzidae) melidae). The most abundant and widespread spe- (for details about M. cuscutae, see Tóth et al., 2004a). cies was H. subferruginea. The species is recorded as All three species were locally common but not harmful specific on field bindweed and Calystegia sepium (L.) for dodders. Weevils from the genus Smicronyx (Co- R. Br. (Convolvulaceae) in Slovakia (Tóth and Tóthová, leoptera: Curculionidae) were found to be the princi- 2006). Females deposited oval, light-red eggs in small pal natural enemies of dodders in Slovakia. Larvae of groups of two to five on the leaf surface of field bind- Smicronyx spp. caused stem galls on field dodder. Such weed (mostly on the underside) from mid-April to the damage prevents flowering and fruiting of field- dod end of May. The larvae fed on leaves from mid-May der vines and destruction of flowers and seeds in other to the beginning of July. The highest number of adults Cuscuta. A total of 877 Smicronyx specimens were was found between 21 May and 11 June. For more de- reared from infested plants during the study. Smicronyx tails of the life history of H. subferruginea, see Tóth jungermanniae (Reich) was the most abundant species, and Tóthová, (2006). The larvae and adults were able accounting for up to 96% of the total number of wee- to almost completely destroy the leaves of field bind- vils reared from field dodder galls. Smicronyx coecus weed plants in some uncultivated habitats. The only (Reich) and Smicronyx smreczynskii Solari were rare common natural enemy of H. subferruginea recorded and accounted for only 5.6% and 1.0%. Larvae of in Slovakia was the egg parasitoid Brachista pungens S. jungermanniae and Smicronyx smreczinskii caused (Mayr) (Hymenoptera: Trichogrammatidae). stem galls on Cuscuta europaea L. and C. campes- tris as well as seed destruction on Cuscuta epithymum (L.) L., and C. europaea. On the other hand, larvae of Common teasel S. coecus were found in flowers and seeds ofC. epithy- Seven insect species were found associated with mum and C. europaea only. Infestation of field dodder common teasel in Slovakia. These were Macrosiphum by Smicronyx spp. ranged between 0% and 100%. rosae (L.) (Sternorrhyncha: Aphididae), Metzneria neuropterella Zeller (Lepidoptera: Gelechidae), Endo- Discussion thenia gentianaeana (Hübner), Diceratura ostrinana (Guenée), Cochylis roseana (Haworth) (Lepidoptera: Larvae of M. albocilia exclusively mined the stems Tortricidae), circumvoluta (Fourcroy) (syn. and root crowns of field bindweed in Slovakia. Spen- cribrumella, cribrella) and Homoeosoma nebulellum cer (1973) as well as Awadallah et al. (1976) stated the (D. and Sch.) (Lepidoptera: ). M. rosae and same. Rosenthal and Buckingham (1982) listed C. ar- D. ostrinana were feeding on leaves and rosettes. Im- vensis and also Convolvulus althaeoides as its hosts. mature stages of other moths occupied the flowerheads. M. albocilia therefore appears to be highly host spe- Although most of the species were rare and caused mi- cific on the target weed. Plants infested by M. albo- nor damage to the host plant, adult moths of E. gentia- cilia looked healthy from the outside during its larval naeana and C. roseana were reared in high numbers stage. The stems started to become weak and dry after from D. fullonum flowerheads. Infestation of flower- pupation within the stems. In addition, exit holes may heads by E. gentianaeana reached almost 100% ev- facilitate infection by diseases (Tóth, 2000). A complex

218 Potential biological control agents of field bindweed, common teasel and field dodder from Slovakia of seven hymenopterous parasitoids was shown to have that Smicronyx species, above all Smicronyx junger- a high impact on the populations of the stem-boring maniae, are very promising biological control agents of fly (Tóth et al., 2004b). Although infestation of field field dodder. bindweed was high, parasitism reduced the agromyzid population by about 77%. In conclusion, M. albocilia could be an important biological control agent of field Acknowledgements bindweed, especially in areas where the plant is inva- The authors wish to thank Dr J. Lukáš for his help sive (e.g. North America), and parasitization of the fly in parasitoid and J. Cunev for weevil identifications. would be expected to be lower. Part of this work was supported by the Grant Agency Seven species of tortoise beetles were collected dur- VEGA, project No. 1/3451/06. ing the surveys in Slovakia. The predominant and only species attacking field bindweed wasH. subferruginea. This species occurs on field bindweed throughout the References Palearctic region (Kismali and Madanlar, 1990) and is unable to complete development on sweet potato Awadallah, K.T., Tawfik, M.F.S. and Shalaby, F.F. (1976) In- (I. batatas; Rosenthal and Buckingham, 1982). In Slo- sect fauna of bind-weed, Convolvulus arvensis L., in Giza, vakia, H. subferruginea was most frequent in warm Egypt. Bulletin de la Société Entomologique d´Egypte 60, and dry regions, less widespread in temperate regions 15–24. and absent from cold regions (Tóth, 2000). In natural Baloch, G.M., Mohyuddin, A.I. and Ghani, M.A. (1967) Bio- logical control of Cuscuta sp. II. Biology and host-plant xerotherm ecosystems, the species often completely range of Melanagromyza cuscutae Hering (Dipt. Agromy- defoliated plants, while in cultivated crops, the beetles zidae). Entomophaga 12, 481–489. were not able to control their host plant. However, CAB (1987) Digest: Potential for biological control of Cus- their effect was clear in vineyards with living green cuta spp. and Orobanche spp. Biocontrol News and Infor- cover. Although predation and parasitization of tortoise mation 8, 193–199. beetles is mentioned as a major factor lowering their Cheesman, O.D. (1996) Life histories of Cochylis roseana populations in the field, except for the egg parasitoid, (Haworth) and Endothenia gentianaeana (Lepidop- B. pungens, no parasitoids of larvae and adults were tera: Tortricidae) on wild teasel. The Entomologist 115, recorded during our study. H. subferruginea was pri- 65–80. oritized for the inundative biological control of field Jehlík, V. (1998) Alien expansive weeds of the Czech Repub- bindweed in Slovakia. lic and Slovak Republic. Academia Praha, Czech Repub- lic, 506 pp. For common teasel, the tortricid C. roseana was se- Kismali, S. and Madanlar, N. (1990) The role of Chrysome- lected as a potential classical biological control agent lidae (Coleoptera) species for the biological control of because of its ability to cause high seed reductions, its weeds and the status of the species in Izmir. In: Proceed- common occurrence in Slovakia and its distinct prefer- ings, 2nd Turkish National Congress of Biological Con- ence for D. fullonum (Cheesman, 1996). While Sforza trol. September 26–29, 1990, Turkey, pp. 299–308. (2002) concluded that C. roseana and E. gentianaeana Rees, N.E and Rosenthal, S.S. (1996) Field bindweed. In: should be similar in their potential as biological control Rees, N.E., Quimby, P.C., Piper, G.L., Coombs, E.M., agents for teasel, our results show that E. gentianaeana Turner, C.E., Spencer, N.R. and Knutson, L.V. (eds) Bio- is not very promising because one larva damaged only logical control of weeds in the West. Western Society of about ten seeds. Weed Science, Bozeman, MT, USA. Parasitic weeds (Cuscuta spp.) only reproduce by Rosenthal, S.S. and Buckingham, R.G. (1982) Natural en- emies of Convolvulus arvensis in western Mediterranean seeds. Thus, complete biological control of these weeds Europe. Hilgardia 5, 1–19. should be achievable by using organisms which damage Sforza, R. (2002) Candidates for the biological control of tea- the seeds. In the absence of species that kill the weeds sel, Dipsacus spp. In: Cullen, J.M., Briese, D.T., Kriticos, at the seedling stage, the suppression of seed produc- D.J., Lonsdale, W.M., Morin, L. and Scott, J.K. (eds) Pro- tion is thus believed to be more important than dam- ceedings of the XI International Symposium on Biological age to individual plants. Research efforts should also Control of Weeds. CSIRO Entomology, Canberra, Austra- be directed to continue investigations on phytophagous lia, pp. 155–161. , which can effectively be combined to pro- Spencer, K.A. (1973) Agromyzidae (Diptera) of Economic vide maximum stress on parasitic weeds. Smicronyx Importance. W. Junk, The Hague, The Netherlands, spp. prevent flowering and fruiting of field dodder, -ei 418 pp. ther directly, through their feeding activity in the seed Tóth, P. (2000) Insects—A Fresh Perspective in the Biologi- cal Control of Field Bindweed (Convolvulus arvensis L.). capsules, or indirectly, through weakening the shoots. PhD thesis. Slovak Agricultural University, Nitra, Slova- If the stem of the species is not attached to its host plant kia, 229 pp. beyond the attacked (galled) part, the entire section is Tóth, P. and Cagáň, Ľ. (2001) Spread of dodder (Cuscuta killed (Baloch et al., 1967). Thus, Smicronyx is able to spp.) in the agroecosystems of Slovakia: is it an emerging cause 100% seed reduction. In addition, they attacked problem? Acta Fytotechnica et Zootechnica, 4 (Special field dodder over the whole growing season. We expect Number), 117–120.

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Tóth, P, Černý, M. and Cagáň, Ľ. (2004a) First records of control of Convolvulus arvensis. Biocontrol News and In- Melanagromyza cuscutae Hering, 1958 (Diptera: Agro- formation 26, 17N–40N. myzidae) from Slovakia and its new host plant. Entomo- Tóth, P., Cristofaro, M. and Cagáň, Ľ. (2005) Seasonal biol- logica Fennica 15, 48–52. ogy of Melanagromyza albocilia (Diptera: Agromyzidae) Tóth, P., Cristofaro, M. and Cagáň, Ľ. (2004b) Bionomy, sea- and seasonal patterns of field bindweed infestation, under sonal incidence and influence of parasitoids of the field field conditions in Slovakia. Entomologica Fennica 16, bindweed stem borer fly Melanagromyza albocilia (Dip- 254–262. tera:Agromyzidae) in Slovakia. In: Cullen, J.M., Briese, Tóth, P. and Tóthová, M. (2006) Possibilities for biologi- D.T. Kriticos, D.J., Lonsdale, W.M., Morin, L. and Scott, cal control of field bindweed (Convolvulus arvensis J.K. (eds) Proceedings of the XI International Symposium L.) by tortoise beetles (Chrysomelidae: Cassidinae). on Biological Control of Weeds. CSIRO Entomology, In: Herda, G, Mazáková, J. and Zouhar, M. (eds) Pro- Canberra, Australia, pp. 351–352. ceedings of XVII Czech and Slovak Plant Protection Tóth, P. and Cagáň, Ľ. (2005) Organisms associated with the Conference. CAU, Prague, Czech Republic, pp. 528– family Convolvulaceae and their potential for biological 532.

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