Prospects for Biological Control of Ambrosia Artemisiifolia in Europe: Learning from the Past
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DOI: 10.1111/j.1365-3180.2011.00879.x Prospects for biological control of Ambrosia artemisiifolia in Europe: learning from the past E GERBER*, U SCHAFFNER*, A GASSMANN*, H L HINZ*, M SEIER & HMU¨ LLER-SCHA¨ RERà *CABI Europe-Switzerland, Dele´mont, Switzerland, CABI Europe-UK, Egham, Surrey, UK, and àDepartment of Biology, Unit of Ecology & Evolution, University of Fribourg, Fribourg, Switzerland Received 18 November 2010 Revised version accepted 16 June 2011 Subject Editor: Paul Hatcher, Reading, UK management approach. Two fungal pathogens have Summary been reported to adversely impact A. artemisiifolia in the The recent invasion by Ambrosia artemisiifolia (common introduced range, but their biology makes them unsuit- ragweed) has, like no other plant, raised the awareness able for mass production and application as a myco- of invasive plants in Europe. The main concerns herbicide. In the native range of A. artemisiifolia, on the regarding this plant are that it produces a large amount other hand, a number of herbivores and pathogens of highly allergenic pollen that causes high rates of associated with this plant have a very narrow host range sensitisation among humans, but also A. artemisiifolia is and reduce pollen and seed production, the stage most increasingly becoming a major weed in agriculture. sensitive for long-term population management of this Recently, chemical and mechanical control methods winter annual. We discuss and propose a prioritisation have been developed and partially implemented in of these biological control candidates for a classical or Europe, but sustainable control strategies to mitigate inundative biological control approach against its spread into areas not yet invaded and to reduce its A. artemisiifolia in Europe, capitalising on past experi- abundance in badly infested areas are lacking. One ences from North America, Asia and Australia. management tool, not yet implemented in Europe but Keywords: common ragweed, non-native ⁄ exotic weed, successfully applied in Australia, is biological control. biological control, integrated weed management, herbi- Almost all natural enemies that have colonised vory, fungi. A. artemisiifolia in Europe are polyphagous and cause little damage, rendering them unsuitable for a system GERBER E, SCHAFFNER U, GASSMANN A, HINZ HL, SEIER M&MU¨ LLER-SCHA¨ RER H (2011). Prospects for biological control of Ambrosia artemisiifolia in Europe: learning from the past. Weed Research 51, 559–573. Introduction economic or ecological effects of biotic invasions in Europe began to increase only recently (Hulme et al., In Europe, as in most other regions of the world, the 2009). Because of this, regulation and management of number of alien plant species has increased considerably exotic species in Europe is less advanced than elsewhere in the past 200 years as a result of increasing trade, (Hulme et al., 2009). Yet, Europe is also suffering from tourism and disturbance (Pysˇ ek et al., 2009). However, invasive species, and a crude estimate of monetary in contrast to North America, South Africa, Australia impact (costs of damage and control) suggests that this or New Zealand, serious concern about the negative exceeds €12 billion annually (Kettunen et al., 2009). Correspondence: Urs Schaffner, CABI Europe-Switzerland, 2800 Dele´ mont, Switzerland. Tel: (+41) 32 4214877; Fax: (+41) 32 4214871; E-mail: u.schaff[email protected] Ó 2011 The Authors Weed Research Ó 2011 European Weed Research Society Weed Research 51, 559–573 560 E Gerber et al. This is an underestimate, as potential economic and This article outlines the present status, impact and environmental impacts are unknown for most of the management of A. artemisiifolia and other exotic alien species found in Europe (Vila` et al., 2010). Ambrosia species in Europe, reviews the available Like no other plant, Ambrosia artemisiifolia L. (com- information on natural antagonists associated with mon ragweed) has raised the awareness of invasive plants Ambrosia species in Eurasia (their introduced range) in Europe. First records of this plant species in western and North and South America (their native range), Europe date back to the mid-1800s and in eastern summarises attempts to control A. artemisiifolia using Europe to 1900, but it was only in the late 1920s that biological control worldwide and explores prospects for A. artemisiifolia became an increasing problem in Europe its application in Europe, including a prioritisation of (Csontos et al., 2010). The main concern regarding potential biological control organisms. A. artemisiifolia is its large production of highly aller- genic pollen that already causes rates of sensitisation Taxonomy and distribution among Europeans ranging from 15% (e.g. Germany, the Netherlands and Denmark) to 60% (Hungary: Rybnicek Ambrosia species are annual or short-lived perennial &Ja¨ ger, 2001; Taramarcaz et al., 2005). This results in plants in the family Asteraceae, placed in the tribe allergic rhinitis and severe asthma in over 20% of the Heliantheae and subtribe Ambrosiinae. Ambrosia is said population of affected areas (Kazinczi et al., 2008). to contain between 21 (Sheppard et al., 2006) and 41 The recent spread of A. artemisiifolia and the result- species (Payne, 1966) worldwide. The genus is thought ing increasing risk to human health and agriculture have to have evolved in the Sonoran desert (south-western resulted in a number of publications on the further USA and adjacent Mexico) and subsequently radiated invasion and potential danger of this invasive weed, its outwards, with species today mainly occurring in North medical aspects, pollen monitoring across Europe and and South America (Payne, 1966). The two species of control methods at a local scale (Buttenschøn et al., main concern to Europe, A. artemisiifolia and Ambrosia 2009). In 2006, the national authorities in Hungary and trifida L., both apparently speciated after the genus had Switzerland established a legal basis for mandatory radiated, and neither species now occurs in the Sonoran control of A. artemisiifolia. Although chemical and desert (Payne, 1964). According to the Global Invasive mechanical control methods have been developed Species Database, the native range of A. artemisiifolia and partially implemented (Buttenschøn et al., 2009), includes Mexico, the United States and Canada (GISD, sustainable control strategies to mitigate spread into 2009). areas not yet invaded and to reduce its abundance in Only one species of the genus, Ambrosia maritima L., badly infested areas are lacking in Europe. One man- is native in Europe, but it is restricted to the Mediter- agement tool that has received little attention in Europe ranean region (Greuter, 2006–2009). Payne (1966) suggested so far is biological control (cf. Mu¨ ller-Scha¨ rer and that A. maritima might be an ecological form of Schaffner (2008), for a recent review on the various A. artemisiifolia, but its species status is now considered methods and strategies and Shaw et al. (2011) for as accepted (Greuter, 2006–2009). Other genera within control of Fallopia japonica). Based on a prioritisation the subtribe Ambrosiinae include Parthenium, Xanthium, scheme developed by Sheppard et al. (2006), A. artemisii- Iva and Heptanthus. With the exception of Xanthium folia was identified as one of the 20 most promising sibiricum Patrin, a species native to Asia (GRIN, 2009), species for classical biological control in Europe. all other species from these genera are native only to Ambrosia artemisiifolia also causes problems in the North and ⁄ or South America (Bremer, 1994). northern parts of North America, Australia and large Several species have been accidentally introduced parts of Asia, so there is a significant amount of into Eurasia, four of which are naturalised in European information available on the biology of this plant and on countries (Table S1). Ambrosia artemisiifolia is the most the efficacy of various control measures. Ambrosia important of the introduced Ambrosia species. This artemisiifolia has been subjected to classical biological species has been recorded from almost all European control programmes in eastern Europe, Australia and countries (DAISIE, 2009; Table S1), but at variable eastern Asia with variable success (Julien & Griffiths, densities. The regions most severely invaded in Europe 1998; Zhou et al., 2009). The information gathered in are central (Hungary, Austria, Slovakia), eastern these biological control programmes may act as a basis (Ukraine, European part of Russia), south-eastern on which to develop a biological control programme for (Romania, Croatia, Serbia) and southern Europe Europe. Integration of biological control into existing (southern France, Italy). In contrast, A. artemisiifolia short-term control measures may then lead to a is currently relatively rare in northern Europe (e.g. sustainable management strategy of A. artemisiifolia Ireland, Scotland, Norway and Sweden), but climate and other Ambrosia species invasive in Europe. change is expected to facilitate the establishment of Ó 2011 The Authors Weed Research Ó 2011 European Weed Research Society Weed Research 51, 559–573 Biological control of Ambrosia in Europe 561 ragweed as a self-propagating weed in these regions in psilostachya is considered to have less potential for the near future (Hyvo¨ nen et al., 2011). establishment and spread in Europe, because it produces Based on molecular markers, populations in France less seeds than the two annual exotic Ambrosia species have been found