The fauna of juncea L. () in and preliminary studies of cognata (L.) (: ) as a potential biological control agent

I. Lecheva,1 A. Karova1 and G. Markin2

Summary Between 2001 and 2005, a survey of rush skeletonweed, L. (Asteraceae), and its associated insect fauna was conducted in Bulgaria. The weed occurs from sea level to 1200 m mainly on roadsides (47% of populations encountered), disturbed and abandoned farmlands (40%), as well as in orchards, vineyards and fields of wheat, roses and lavender. For the first time in Bulgaria, the insect species associated with the were inventoried. A total of 51 insect species were collected, but only four appeared to be specific to the plant. The most dominant species and the one considered most promising as a potential biological control agent was the , Fr. (Lepidoptera: Noctuidae). S. cognata larvae feed on the reproductive parts of the plant, and during development, one larva can consume 61 to 62 flower buds or seed heads. In Bulgaria, the moth has two generations that overlap, with maximum population densities in July and August. S. cognata is widely distributed throughout Bulgaria and was found in high densities in most of the populations of C. juncea studied. It was not observed attacking any other native plant or cultivated , and preliminary host-range studies of four closely related species indicated that it could only feed and develop on C. juncea. S. cognata has therefore been selected as a potential biological control agent for possible future intro- duction in .

Keywords: Schinia cognata, host-range testing, rush skeletonweed, distribution.

Introduction some areas of Washington (Piper and Andres, 1995). However, in the cooler interior states of Oregon, Idaho Rush skeletonweed, Chondrilla juncea L. (Asteraceae), and Montana, the three agents have not given effective has been accidentally introduced in northwest USA and control. A new program was implemented to determine adjacent Canada, and in Argentina and Australia and if new and more effective biological control agents in all areas, it has become a major noxious weed. In could be found in Eurasia (Markin and Quimby, 1997). Australia, a program in the 1970s resulted in the suc- As part of this program, a study on C. juncea-associated cessful introduction of three biological control agents phytophagous to identify potential biocontrol that soon controlled C. juncea over most of its range agents was conducted in Bulgaria in 2000 to 2005 (Cullen and Groves, 1977). A similar program by the (Karova and Lecheva, 2005, Karova, 2006). Agricultural Research Service of the US Department of Agriculture introduced and established the same three agents in North America and resulted in satisfac- Methods and materials tory control of the weed in the state of California and From 2000 to 2005, field visits were made to all regions of Bulgaria to determine the distribution, main habi- 1 Agricultural University of Plovdiv, Faculty of Plant Protection and tats, population densities and phenology of C. juncea. Agroecology, 12 Mendeleev Str., Plovdiv 4000, Bulgaria. When stands of C. juncea were encountered, the plants 2 USDA Forest Service, Rocky Mountain Research Station Forestry Sci- were visually examined, and all associated insects col- ences Laboratory, Bozeman, MT, USA. Corresponding author: I. Lecheva . lected. Samples of flower buds, stems and roots were © CAB International 2008 also collected and dissected. Individuals collected as

301 XII International Symposium on Biological Control of Weeds larvae were reared in the laboratory using potted C. Table 1. Frequency distribution by habitat of 84 stands of juncea plants or using the appropriate plant part in Chondrilla juncea found in a survey of Bulgaria plastic cages or Petri dishes, and adults that emerged between 2001 and 2005 (Karova and Lecheva, were identified. 2005; Karova, 2006). From this survey, the most common and destructive Habitats in which Percent of stands insect encountered was the moth, Schinia cognata Fr. Chondrilla juncea (Lepidoptera: Noctuidae), which was selected for more was found detailed studies. Laboratory studies of the development Road sides 46.75 and feeding behaviour of S. cognata were conducted Abandon farmland 39.4 at the facility of the Department of Agri-Ecology and Fallow wheat fields 4.25 Entomology of the Agricultural University of Plovdiv Grape vineyards 4.25 a (Bulgaria). Observations on the seasonal population Fields of roses 1.06 a dynamics of S. cognata were conducted on two popu- Fields of lavender 1.06 lations near Plovdiv in central Bulgaria in 2003 and Other locations 4.27 2004, using sweep netting. The sites were visited eight a Fields of ornamental roses (Rosa spp.) (Rosaceae) and lavender times during each summer, and five batches of 100 (Lavandula officinallis L.) (Labiatae) are extensively grown in Bulgaria as a source of fragrance. plants swept with a 37-cm diameter canvas sweep net. The sampling was carried out primarily to determine juncea were usually other weed species such as Cicho- the abundance of S. cognata adults and larvae, but all rium intybus L. (Asteraceae), Chamomilla recutita (L.) other insects collected were also counted to provide Rauschert (Asteraceae), Avena fatua L. (Poaceae), Cus- an estimate of their relative abundance (percent of all cuta spp. (Convolvulaceae), Cirsium arvense (L.) Scop. insects collected over the 2 years). To determine the (Asteraceae), Centaurea cyanus L. (Asteraceae) and potential host range of S. cognata, other plant species Verbascum thapsus L. (Scrophulariaceae). of Asteraceae growing adjacent to attacked C. juncea The vegetative growth of rush skeletonweed in Bul- plants were searched for S. cognata larvae. garia begins at the end of March and the first weeks of Laboratory feeding tests were conducted using field April depending on the local climatic conditions and collected early instar larvae or larvae reared from eggs. altitude. Flower buds are formed at the beginning of We determined the development and feeding impact June, and flowering was observed at the end of the same (number of reproductive structures consumed) of lar- month; by November, the flowering stem had died. vae held on potted plants and bouquets of plants, cov- ered by transparent plastic screen cages. Choice feeding Phytophagous insects feeding tests used bouquets of C. juncea intermixed with a test plant with their bases wrapped in cotton, placed in small on C. juncea tubes of water and held in plastic screen cages. For During the 5 years of the survey, a total of over no-choice feeding tests, the reproductive parts of the 51 insect species from Coleoptera, Lepidoptera, Het- plant being tested were offered to larvae held in a 20 ´ eroptera, Homoptera and Diptera were found associ- 1.5 cm glass Petri dish. Reproductive parts were re- ated with C. juncea. The species found, their density placed when consumed or wilted until either the larvae and seasonal occurrence has been presented elsewhere pupated or died. All choice and no-choice tests were (Karova and Lecheva, 2005; Karova, 2006). Most of the replicated ten times using one larva each. For these identified species were moth larvae, leaf beetles, plant preliminary host tests, four locally available species of bugs and other sucking insects. To a lesser extent, the closely related Asteraceae were used. flower buds, flowers and seed heads of C. juncea were damaged by plant bugs, Lepidoptera larvae and beetles. Only two species were recovered from the roots: larvae Results and discussion of the moth, gilveolella Tri. (Lepidoptera: Distribution, habitats, population density ), which feeds in a sand-encrusted silken case on the outside of the root, and the beetle Mordelistena and phenology of C. juncea micans Germ. (Coleoptera: Mordellidae), the larva of C. juncea is widespread throughout Bulgaria and was which mines down the central core of the root. Most of found in 23 of the 26 regions (=states; Karova and Lech- the species are generalists and thus cannot be consid- eva, 2005). It occurs mainly on roadsides and disturbed ered as potential biocontrol agents. Only four species lands and also in orchards, grape vineyards and fields of appeared to have a restricted host range: B. gilveolella, wheat, lavender and roses (Table 1). It was found from 0 M. micans, the midge Rub. (Dip- to 1200 m above sea level. The densest populations (50 tera: Cocidomidae) and the flower-feeding moth, S. plants/m2) were observed on abandoned farmland around cognata Fr. (Lepidoptera: Noctuidae). B. gilveolella the cities of Plovdiv, Varna, Ihtiman and Dupnitza and and C. schmidti have already been studied and intro- nearly as dense populations (25 to 50 plants per square duced as biological control agents in Australia and the meter) in Blagoevgrad. Other plants occurring with C. USA (Julien and Griffin, 1998; Piperet al., 2004). Min-

302 The insect fauna of Chondrilla juncea L. (Asteraceae) in Bulgaria and preliminary studies of Schinia cognata ing by M. micans appears to have no effect on the plant, Field collected larvae of S. cognata in flower buds of so we concentrated most of our effort on studying S. C. juncea were most abundant not only in the vicinity cognata. of Plovdiv but were also recovered in most regions of the country. Very little previous information exists on S. cognata. According to Nowacki and Fibiger (1996) S. cognata and Rakosy (1996), it occurs in the European part of Among all recovered insect species in Bulgaria, the former USSR, Czech Republic, Austria, Hungary, the seed-head-feeding moth, S. cognate, was the most Former Yugoslavia, , and Bulgaria. The abundant and damaging and seemed the most prom- first record of S. cognata in Bulgaria was from Bah- ising candidate for biological control of C. juncea. It metev (1902) who found only single individuals. Until represented 20% to 34% of all the insects collected now, the moth was considered a rare species. The re- in sweeping the plants in 2003 and 2004 (Table 2). sults of our study show that it has two generations per

Table 2. Relative abundance of insects collected on Chondrilla juncea by sweep netting over the summer of 2004 at two locations near Plovdiv, Bulgaria. Over 50 species were collected (Karova and Lecheva, 2005; Karova, 2006), but only these were observed or suspected of actually feeding on the plant. and species Family Feeding site Percent abundance Coleoptera Gastrophysa polygoni L. Chrysomelidae Foliage 0.95 Cassida nebulosa L. Chrysomelidae Foliage 1.09 Clytra novempunctata L. Chrysomelidae Flower Occ.a Coptocephala rubicunda Laich Chrysomelidae Foliage Occ. Coptocephala unifasciata Scop. Chrysomelidae Foliage Occ. Cryptocephalus connexus Ol. Chrysomelidae Foliage/Flower 2.45 Cryptocephalus sericeus L. Chrysomelidae Flower 3.59 Epicometis hirta Poda. Scorabaeidae Flower 1.63 M. micans Germ.b Mordellidae Roots 0.85 Mylalris polymorpha Pall. Meloidae Pollen 10.17 Zonabris polymorpha Pall. Meloidae Pollen 10.76 Lepidoptera Tr.b Pyralidae Roots Occ. trabealis Scop. Noctuidae Foliage 10 muricata Hufn. Geometridae Foliage 1.24 Melitaea didyma Esp. Nymphalidae Flower 10.26 Plusia gamma L. Noctuidae Flower 0.67 S. cognata Fr. Noctuidae Flower bud 27.15 Simira nervosa (Den. & Schiff.) Noctuidae Foliage 0.81 Adelphocorvis lineolatus Goez. Miridae Sap feeding 4.29 Brachycoleus decolar Renter Miridae Sap feeding 1.25 L. Sap feeding 3.41 Eurybema oleraceae L. Pentatomidae Sap feeding Occ. ornata L. Pentatomidae Sap feeding Occ. Lygus equestris L. Lygaeidae Sap feeding Occ. Lygus pratensis L. Lygaeidae Sap feeding Occ. Lygus rugulipennis Popp. Lygaeidae Sap feeding Occ. Syramastes rhombeus L. Lygaeidae Sap feeding 1.46 Homoptera Aphis spp. Aphididae Sap feeding 2.45 Philaenus spumarius L. Cereopidae Sap feeding 5.45 Diptera C. schmidti Rub.b Cecidomiidae Under cuticle Occ. Dasyneura sp. Cecidomiidae Flower Occ. a Occ. = Occasionally found, but were generally rare or found for only a very short period during the summer b These insects were rarely collected as adults during sweep netting, but their larvae were found on or in the plants.

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Figure 1. Season population density (determined by 5 ´ 100 sweeps with a collection net) of larvae and adults of Schinia cognata near Plovdiv, Bulgaria in 2003 and 2004.

year that overlap, with maximum population densities tuce), and Sonchus oleraceus L. In all choice trials, the in July and August (Fig. 1). The moth overwinters as a larvae fed only on C. juncea, and there was no feed- pupa, and emergence begins in early June. The females ing on the four tested plants. In the no-choice trials, lay their eggs singly on the upper parts of the stems, where the larvae were forced to feed on plants different flower buds and flowers of the host plant beginning in from C. juncea, some larvae attempted to feed but none mid-June. The eggs begin to hatch in the first weeks of survived to pupate. On C. juncea, larvae development July. In the two populations examined near Plovdiv, the was normal; most of them pupated and adults emerged highest density of larvae was observed in mid-July and successfully. mid-August. The larvae feed on the reproductive parts of C. juncea, i.e. flower buds, flowers and seed heads. Conclusion Observations under laboratory conditions showed that, for full development, one larva consumes 61 to 62 Among the insect species found feeding on C. juncea flower buds, flower heads or seed heads. in Bulgaria, the dominant species was the moth S. cog- During our investigations, the moth was not encoun- nata. The larvae feed on the reproductive parts of the tered on other related weed species or cultivated plants plant and were observed to cause extensive damage growing in the vicinity of attacked C. juncea plants. in the field. S. cognata is widely distributed, occurs at Laboratory feeding tests confirmed its host specificity. high densities in all C. juncea population studies and Four closely related species of Asteraceae were used was not recorded or observed feeding on other, local or for both choice and no-choice trials: C. intybus L., cultivated plants. It could not be reared on four closely Lactuca serriola L., Lactuca sativa L. (domestic let- related plant species and is therefore considered a po-

304 The insect fauna of Chondrilla juncea L. (Asteraceae) in Bulgaria and preliminary studies of Schinia cognata tential biocontrol agent. Arrangements have been made as agents for biological control. PhD Dissertation. Agri- to ship colonies of S. cognata to a plant containment cultural University of Plovdiv, Plovdiv, Bulgaria, 137 pp. facility in Bozeman, Montana in the USA where it can (in Bulgarian). undergo more extensive host testing on North Ameri- Karova A. and Lecheva, I. (2005) Study on the habitats of can crops and native species. Chondrilla juncea L. (Asteraceae) and the diversity of its natural enemies in Bulgaria. Plant Sciences 42, 456–460 (in Bulgarian). Acknowledgements Markin G. and Quimby, P. Jr. (1997) Report of work on biological control of rush skeletonweed (Chondrilla jun- We would like to thank the USDA-ARS, European cea). Unpublished report on file at USDA Forest Service, Biological Control Laboratory, Montpellier, France, Forestry Sciences Laboratory, MSU Campus, Bozeman, and USDA Forest Service, Rocky Mountain Experi- Montana, p. 37. ment Station, Fort Collins, Colorado, U.S.A., for the Nowacki, J. and Fibiger, M. (1996) Noctuidae. In: Karsholt, successful collaboration and financial support. O. and Razowski, J (eds) The Lepidoptera of . Apollo, Stenstrup, Denmark, pp. 251–293. Piper, G.L. and Andres, L.A. (1995) Rush skeletonweed. In: References Nechols, J.R., Andres, L.A., Beardsley, J.W., Goeden, R.D. and Jackson, C.G. (eds) Biological Control in the Bahmetev, P. (1902) Babochki Bolgarii. Trudui Rossijskoi Western United States. University of California. Division Entomologicheskoi Obshtestva Sankt-Petersburg, 35, of Agriculture and Natural Resources. Publication 3361, 356–466. pp. 252–255. Cullen, J.M. and Groves, R.H. (1977) The population biology Piper, G.L., Coombs, E.M., Markin, G.P. and Joley, D.B. of Chondrilla juncea L. in south-eastern Australia. Jour- (2004) Rush skeletonweed. In: Coombs, E.M., Clark, nal of Ecology 54, 345–365. J.K., Piper, G.L. and Confrancesco, Jr., A.F. (eds) Bio- Julien, M.H. and Griffiths, M.W. (1998) Biological Control of logical Control of Invasive Plants in the United States. Weeds: A world catalogue of agents and their target weeds, Oregon State University Press, Corvallis, OR, pp. 293– 4th edn. CABI Publishing, London, England, 223 pp. 303. Karova, A. (2006) Study on Chondrilla juncea L. (Astera- Rakosy, L. (1996) Die Noctuidae Rumaniens (Lepidoptera, ceae), associated phytophagous insects and their potential Noctuidae). Druckerei Gutenberg, Linz–Dornach, 648 pp.

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