Feasibility of biological control of common ragweed () a noxious and highly allergenic weed in Europe

Conveyors: D. Coutinot,1 U. Starfinger,2 R. McFadyen,3 M.G. Volkovitsh,4 L. Kiss,5 M. Cristofaro6 and P. Ehret7

Introduction • reported impacts of A. artemisiifolia in several Eu- ropean countries on human health, plant health and Established in Europe for more than a century, the com- nature conservation, mon ragweed, Ambrosia artemisiifolia L., is the most • expressed their concern about an ongoing spread of polluting invasive weed causing allergies to European the species in Europe, populations in various countries and is causing enor- • urged authorities in countries concerned to prevent mous health costs. At present, there is no effort from further import and spread or to control existing pop- European decision makers to implement biological con- ulations, trol at the European level against common ragweed. • gave a set of recommendations for all private or public bodies concerned. Presentation of results of the international The experts considered biological control as an im- meeting of experts, Vienna (AGES), portant tool in the strategy of managing A. artemisi- 27 September 2006 (Uwe Starfinger) ifolia: On the invitation of BBA, Braunschweig, and • A. artemisiifolia is a suitable target for biological AGES, Vienna, experts from the fields of agronomy, control in natural, ruderal and settlement areas, as botany, ecology, plant protection and road maintenance well as along traffic ways. from seven European countries gathered for a one-day • From a risk assessment point of view, the sub-tribe workshop to discuss the problems caused by Ambrosia Ambrosiineae does not include crop species in artemisiifolia and the availability and effectiveness of Europe. control measures. Results and individual contributions • The risk to A. maritima, the only native species of are published at the BBA website (www.bba.bund.de/ the sub-tribe in Europe, has to be assessed. ambrosia). In particular, the experts • Success of biological control of a closely related species () and A. artemi- siifolia in Australia is a good argument to establish biological control in Europe. 1 European Biological Control Laboratory, USDA–ARS, Campus Inter- • Additional suitable biological control agents have national de Baillarguet, CS 90013 Montferrier-sur-Lez, 34988 St. Gely been identified in the native area ofA. artemisiifolia du Fesc, France . and have to be investigated further. 2 Biologische Bundesanstalt für Land und Forstwirtschaft, Abteilung für nationale und internationale Angelegenheiten der Pflanzengesundheit, A follow-up meeting is planned for 2008 at the next Messeweg 11/12, 38104 Braunschweig, Germany . 3 CRC for Australian Weed Management, Block B, 80 Meiers Road, In- dooroopilly, QLD 4068, Australia Success of biological control against 4 Laboratory of Systematics, Zoological Institute of the Russian Academy of Sciences, Universitetskaya Embankment 1, St.Petersburg common ragweed in Australia 199034, Russia . (Rachel McFadyen) 5 Plant Protection Institute, Hungarian Academy of Sciences, H-1525 Budapest, PO Box 102, Hungary . Artemisia artemisiifolia is classified as a declared 6 ENEA-BIOTEC/BBCA, Lgo. Santo Stefano, 3 Anguillara Sabazia, ‘class 2’ weed in two eastern states of Australia: ‘can po- Rome 00061, Italy . tentially cause substantial economic and environmental 7 DGAL/SDQPV, Ministère de l’Agriculture et de la Pêche, DRAF/ SRPV ZAC d’Alco, BP 3056 34034 Montpellier, France . keep their land free of these weeds.’ Biological controls

717 XII International Symposium on Biological Control of Weeds have been implemented as a management option for in North America. Certain of these have already been ragweed in Australia. Several insect species have been introduced and established within the framework of a introduced for biological control of common ragweed, classical biological control against Ambrosia in vari- two of which are established and giving good control. ous countries but never in Europe. The list of all re- The leaf-feeding bicolorata Pallis- leased biological control agents was presented during ter (Coleoptera: Chrysomelidae) was introduced from the workshop; the list below is those who have been Mexico in 1980 as a biocontrol agent for the weed reported as established: Parthenium hysterophorus L. (). Defoliation has immediate negative effects on plant performance strenuana (Walker) (: Tortric- and as a consequence affects the growth, reproduction idae) and fitness of the plants. In some locations and years, Introduced from Mexico in 1982 in Australia where Z. bicolorata caused 85–100% defoliation, resulting it is widely established. in significant reductions in plant density, growth and Introduced from Mexico in 1991 in China: under flower production. East coast areas receiving greater evaluation. and more frequent rainfall had higher weed density and consequently higher beetle density. The stem- Zygogramma bicolorata Pallister (Coleoptera: Chryso- galling Epiblema strenuana (Walker) (Lepidop- melidae) tera: ) was introduced from Mexico in 1982 Introduced from Mexico in 1980 in Australia where for biological control of P. hysterophorus and became it is well established. widely established within 2 years of introduction. E. strenuana now occurs throughout the range of its Zygogramma disrupta Rogers (Coleoptera: Chrysome- host plants parthenium, Noogoora burr ( lidae) occidentale Bertol.) and annual ragweed (A. artemisi- Introduced from the US in 1990 in Russia; the spe- ifolia L.) in Australia. Galls can kill seedling plants and cies is under evaluation. severely reduce growth of larger plants, and as a result annual ragweed is no longer a serious weed in eastern Zygogramma suturalis (Fabricius) (Coleoptera: Chrys- Australia. omelidae) Introduced from Canada & US in 1978 in the Repub- Biological control of common ragweed, lic of Georgia and released in Abhazia (West Georgia) Ambrosia artemisiifolia L. in Russia and Lagodekhi region (East Georgia): the establish- ment needs to be confirmed and evaluated. (Mark Volkovitsh) Introduced from Canada & US in 1978 in Ukraine: The ragweed , Zygogramma suturalis F. establishment is not confirmed. Introduced from Canada was introduced to Russia from the USA and Canada in & US in 1978 in Russia, where the species is estab- 1978 to control the common ragweed, Ambrosia arte- lished. Introduced from US in 1985 in the ex Yugoslavia, misiifolia. The initial phase of this introduction was a where establishment needs to be evaluated. population explosion with more than a 30-fold yearly Introduced from Canada in 1988 in China, where it increase in number and population density (up to 5000 was recovered in some provinces. Introduced from US adults/m2 in aggregations). in 1980 in Australia, but not established. In 2005–2006, we conducted selective quantitative sampling over the whole area infested by A. artemi- The use of insect biological control agents within siifolia in southern Russia. The average population the framework of a classical biological control program density of the ragweed leaf beetle was very low: 0.001 against Ambrosia does not seem to be under consider- adults/m2 in crop rotations and 0.1 adults/m2 in more ation to date by decision-makers in Europe. stable habitats. In an overwhelming majority of in- spected populations, the impact on the targeted weed was negligible. However, having regard to the spectac- List of potential fungal biological ular success achieved in the permanent experimental control agents for Ambrosia artemisiifolia plot in 1983–1985, it is still possible that stable pro- & Species under consideration in Hungary tected field nurseries could be a promising method ofZ. (Levente Kiss) suturalis propagation for biological control of ragweed in surrounding areas. There are several fungal pathogens of common rag- weed (A. artemisiifolia) that have already been con- List of the known insect biological control sidered as potential biological control agents of this noxious weed. Protomyces gravidus, causing an en- agents (Dominique Coutinot) demic stem gall disease on giant ragweed (A. trifida) in Many potential insect biological control agents ex- the USA, was evaluated as a potential mycoherbicide ert a pressure on Ambrosia in its native environment against both giant and common ragweed. A Phoma sp.

718 Feasibility of biological control of common ragweed isolated from A. artemisiifolia in Canada performed • host specificity studies of the potential selected can- well in inundative experiments alone and especially in didate , combination with a leaf-eating beetle, Ophraella com- • selection of one or more (specific) plant-pathogens muna. Puccinia xanthii, a microcyclic autoecious rust (fungi), reported to infect common ragweed in some parts of • insect–pathogen interaction studies, the USA, was proposed as a classical biological control • evaluation of the impact of potential agents on the agent outside North America. To our knowledge, none weed in a confined field environment, of these, or any other fungal pathogens, are currently • evaluation of potential synergisms with herbicides, investigated as potential biological control agents of • development of an information and educational A. artemisiifolia except a strain of Sclerotinia scleroti- network. orum, which is under consideration as a mycoherbicide In conclusion, real eradication (or at least suppression) in Hungary. of the target weed can be achieved only if Italy becomes involved together with other European Countries in an Biocontrol of Ambrosia artemisiifolia in integrated network, using biological control in combi- Hungary: ideas, options and problems nation with other different agronomic and mechanical strategies. Currently, Hungary is the country where the air is most polluted with ragweed pollen in Europe. Agri- cultural and other control measures have not helped to Phytosanitary status of reduce the amount of this airborne allergen so far. Clas- Ambrosia artemisiifolia— sical biocontrol of ragweed could be a feasible way to a few examples (Pierre Ehret) achieve this goal because most of the natural enemies of A. artemisiifolia, known to occur in its native areas Experts participating on the workshop to discuss the in North America, are missing from Europe. Puccinia problems caused by Ambrosia artemisiifolia in Vienna xanthii, a microcyclic autoecious rust reported to infect in 2006 recommended that ‘countries should explore common ragweed in some parts of the USA, as well legal possibilities to regulate Ambrosia’. as two leaf-eating , Zygogramma suturalis and It is clear that, because of its extremely large geo- Ophraella communa, have already been proposed as graphic distribution, this weed does not fit with quar- classical biological control agents of ragweed in Hun- antine regulations in most parts of the world. Different gary. In addition, a mycoherbicide product based on a types of ‘official control’ and different levels of deci- strain of Sclerotinia sclerotiorum is under development sion (national, regional or local) do exist nevertheless. in Hungary. Some are in the phytosanitary field; more are related to health or more global environment fields. Species under consideration in Italy Local or regional approach is well adapted to an al- ready widespread weed, and biological control seems (Massimo Christofaro) to warrant further exploration as part of the portfolio of Ragweed, Ambrosia artemisifolia, an alien weed that control methods. originated from America, is now infesting the Po Val- ley regions in Italy. Due to the regional distribution of the plant, Italy lacks national legislation for the preven- Discussion tion and control of A. artemisiifolia. In northern Italy, regional governments as well as single municipalities Biological control could be one of the tools to control have issued local laws and guidelines that establish: common ragweed in Europe. Taking advantage of the • mandatory mowing in late June, late July and mid examples from Australia and Russia with insect biolog- August ical control agents, further investigation and research • general guidelines for early warning in urban areas, on rust and other weed pathogens needs to be devel- • improvement of the pollen monitoring station system. oped at a European level. Although the total eradica- tion of this plant is not feasible, a European program In the Lombardy region alone, the direct costs of A. for the biological control of common ragweed would artemisiifolia allergies on the public health system ex- be highly desirable. ceed 1 million euros (2003). This workshop had as objective to reply to the con- Mainly because of its alien origin and the territory clusions of the experts at the workshop organized in occupied, biological control can be considered a fea- Vienna by OLD (AT) and BBA (OF) at the NEOBIOTA sible approach. The following specific steps would be conference. The presentations and conclusions provide required: a basis for forthcoming discussions in future scientific • evaluation of of A. artemisiifolia distribution in Italy, or political conferences on the management of com- • genetic characterization of weed and insect popula- mon ragweed including the feasibility of a biological tions in Italy and North America, control program against Ambrosia in Europe.

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