DOI: 10.1111/j.1365-3180.2011.00879.x

Prospects for biological control of Ambrosia artemisiifolia in Europe: learning from the past

EGERBER*,USCHAFFNER*,AGASSMANN*,HLHINZ*,MSEIER & 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.

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]

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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 Biological control of Ambrosia in Europe 3 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 to have similar genetic variability as (EPPO, 2009). those in North America, but within-population varia- tion was surprisingly higher in the introduced than in the Impact and management native range (Genton et al., 2005). Indeed, multiple sources of the French populations were diagnosed, but Impact on human health subsequent analyses showed that this was rather the result of introduction of seed mixtures containing Ambrosia species produce allergenic pollen, which can different North American populations than due to induce allergic disease, such as rhinitis, conjunctivitis and multiple introductions (Genton et al., 2005). The intro- asthma, as well as contact dermatitis and urticaria (e.g. duced range of two other species originating from North Taramarcaz et al., 2005; Kazinczi et al., 2008). A clear America, A. trifida and Ambrosia psilostachya DC, correlation was found between the amount of airborne includes several European countries (EPPO, 2009; pollen and the proportion of allergic response in the Table S1). A fourth species, Ambrosia tenuifolia Spreng., population (Ja¨ ger, 2000), with a threshold value of c. 10 native to South America, is recorded from three pollen grains per m3 provoking allergic rhinitis in European countries (Table S1). In addition to these sensitive persons, compared with 50 grass pollen grains four species, a single occurrence is reported for Ambrosia (Taramarcaz et al., 2005). The medical costs of these acanthicarpa Hook from the UK (GBIF, 2009). allergies are already substantial in highly infested regions in Europe, such as in Hungary (110 million € per year; Kazinczi et al., 2008) and Austria (88 million € per year; Biology and dispersal S. Ja¨ ger, HNO–Klinik, Med-UniWien, pers. comm.). Ambrosia artemisiifolia is an annual pioneer species and Besides financial losses because of expensive anti- flourishes in disturbed habitats, such as roadsides, waste allergy treatments, lost working time caused by places, construction sites, agricultural fields, disturbed debilitating allergic reactions constitutes an additional or abandoned fields, waterways and urban areas significant economic cost to society. In highly infested (Fumanal et al., 2008). This wind-pollinated monoe- regions, A. artemisiifolia has rapidly become the main cious plant has been assumed to be self-compatible and allergen, as it is in North America, where its pollen has capable of selfing (Bassett & Crompton, 1975; Genton been reported to account for 50–75% of pollen allergies et al., 2005), but more recent studies using allozyme (Frenz, 1999). Because of its late flowering, pollen affects markers demonstrated high outcrossing rates and strong allergic individuals at a time when many would normally self-incompatibility mechanisms (Friedman & Barrett, be experiencing relief from their symptoms. Ambrosia 2008). The plant overwinters as seed that germinates in species thus extend the Ôproblem seasonÕ of the pollen- spring. Plants are in the vegetative phase from May to allergic population. As a further consequence of its wide August and bloom from August to October (Brandes & distribution and severe impact on human health, tourism Nitzsche, 2007). Pollen production recorded for individ- can be affected if visitors avoid areas with high Ambrosia ual A. artemisiifolia plants collected in France ranged occurrence (e.g. the Dalmatian coast in Croatia). from 4 million to 10 billion grains and seed production from 346 to 6114 seeds per plant (Fumanal et al., Impact on agriculture 2007a). Ambrosia artemisiifolia has a long-term persist- ing seedbank, with seeds remaining viable for more than In Europe, A. artemisiifolia is mainly reported as a weed 39 years (Bassett & Crompton, 1975). of spring-sown crops, causing significant yield losses, Dispersal by seed occurs mostly by human activities especially in sunflower, maize, sugar beet, soyabeans and through soil and seed transport (Bassett & Crompton, cereal crops (Kazinczi et al., 2008). Damage is especially 1975). In addition, seeds can float and hydrochory high in crops with low canopy height, such as beets, appears to be an important dispersal mechanism along which can have up to 70% yield loss (Buttenschøn et al., rivers, explaining the rapid colonisation of newly formed 2009). Because of its late emergence, A. artemisiifolia sand and gravel bars (Fumanal et al., 2007b). Ambrosia can also establish and reach high densities during inter- trifida L. is also an annual weed, and its biology is crop periods in oilseed rape or cereal stubbles, as well as similar to that of A. artemisiifolia, but it is more frost- on fallow and set-aside land (Kazinczi et al., 2008). In resistant, develops faster and its mature seeds appear South Hungary and East Croatia, it is economically the earlier (EPPO, 2009). Ambrosia psilostachya and most important weed in sunflower and soyabean, A. tenuifolia Spreng. are perennial species. Ambrosia causing highest yield reductions and control costs

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(Buttenschøn et al., 2009). The species is particularly from flowering and setting seeds. In non-agricultural problematic for Hungary, where sunflower is a major land, eradication of A. artemisiifolia using herbicides crop plant, and where A. artemisiifolia was present on can be envisaged (Gauvrit & Chauvel, 2010), but often 5.4 million ha in 2003, of which 700 000 ha were heavily financial constraints and the need to protect the accom- infested (To´ th et al., 2004). Yield losses alone were panying vegetation do not allow large-scale application estimated at €130 million per year for Hungary of herbicides. Here, as well as in crops, the management (Ke´ mives et al., 2006). Furthermore, herbicide use is of a competitive plant cover (the crop or the native greatly limited in sunflower because of its botanical vegetation) was found to reduce the biomass of similarity with the weed. The occurrence of A. artemis- A. artemisiifolia effectively, but again, seed set could iifolia in sunflower crops further facilitates the dissem- not be prevented (Buttenschøn et al., 2009). ination of the plant throughout Europe, mainly as bird Thus, effective short-term control measures that seed and crop seed. In addition, widespread herbicide reduce the biomass of A. artemisiifolia are available resistance (e.g. Kazinczi et al., 2008) and the ban or dose for most crop species. However, flowering (including reduction of efficient herbicides greatly limit successful pollen production) and seed set and thus population short-term management in crop fields. propagation of A. artemisiifolia cannot be prevented at present. The large area already invaded by A. artemisii- folia in Europe and the fact that grassland communities, Impact on biodiversity open habitats and riverbanks are increasingly invaded As a pioneer species, A. artemisiifolia is a species (DAISIE, 2009) will not only increase the impact on primarily of secondary succession. It is generally domi- human health, but also on major crops across Europe, nant in undisturbed areas only in the first year of rendering this plant invader economically significant. colonisation, but then, because of its late emergence, it is Sustainable control strategies to mitigate its further replaced by perennial species (Buttenschøn et al., 2009). spread into areas not yet invaded and to reduce its In early successional fields, dense layers of A. artemisii- abundance in badly infested areas are therefore urgently folia in spring can temporarily reduce the number of needed in Europe. One alternative management option, native species, but this effect disappears again later in already successfully implemented in several countries, is the season (Armesto & Pickett, 1985). In general, the biological control. habitat preference of A. artemisiifolia makes most hab- itats of high nature conservation value unsuitable for the Antagonists of Ambrosia artemisiifolia species, but colonisation of dry and semi-dry grassland, open steppe vegetation, sand dunes and embankments To assess whether any natural enemies (herbivores or along rivers has been reported (Brandes & Nitzsche, fungal pathogens) attacking A. artemisiifolia in its 2007). introduced range in Eurasia could be used in a system management approach in Europe or in an inundative approach using native antagonists, we conducted a Current management of Ambrosia species literature survey using the ÔCAB AbstractsÕ and Prevention of invasion is the most cost-effective measure Ôscholar.google.comÕ databases in August 2009, using against plant invaders. The alarming figures outlined the search terms ÔAmbrosiaÕ or ÔragweedÕ, in combination earlier prompted some authorities to react quickly by with ÔherbivoreÕ or ÔinsectÕ or ÔpathogenÕ or Ônatural establishing awareness-raising programmes and guide- enem*Õ or Ôbiological controlÕ, with no restriction on lines for prevention, early detection and rapid response publication year. From all retrieved papers, we also (Buttenschøn et al., 2009). This includes information and screened the reference lists for other suitable publica- awareness campaigns, limiting unintentional spreading tions. A similar search was conducted for the native of A. artemisiifolia seeds and monitoring areas prone to range to compile a comprehensive list of herbivores and invasions, such as along transport corridors. pathogens associated with A. artemisiifolia and other However, the ability of A. artemisiifolia to grow side Ambrosia species, as background data for a potential branches after partial control and its high multiplication classical biological control approach or an inundative rate renders control challenging. Herbicides and approach using exotic biological control agents. mechanical control (uprooting, cutting and ploughing) are best suited as local and short-term measures to Herbivores and pathogens associated with Ambrosia eradicate initial and small populations and to mitigate artemisiifolia in Eurasia further spread of established populations. Herbicide treatments in crops may be sufficient to prevent yield In total, the literature review revealed some 40 insect losses, but cannot prevent A. artemisiifolia populations species (including two unidentified geometrids) associated

Ó 2011 The Authors Weed Research Ó 2011 European Weed Research Society Weed Research Biological control of Ambrosia in Europe 5 with A. artemisiifolia in Eurasia (Table S2). Most of subtribe Ambrosiinae) revealed 109 specialist inverte- these insect species are polyphagous, and they appear to brate (Table S3) and 19 specialist fungal species (Table cause only moderate damage to A. artemisiifolia. The S4). This amounts to c. 36% and 25% of the total only exception is the moth Ostrinia orientalis Mutuura & number of invertebrates and fungal species recorded Munroe (Lepidoptera: Pyralidae), which was found to from the native range respectively. Within invertebrates, significantly reduce biomass and plant height of Lepidoptera (40 species) largely dominate, followed by A. artemisiifolia in China (Wan et al., 2003); however, Coleoptera (28 species), Diptera (19 species) and this species is also recorded from Xanthium sibiricum Hemiptera (18 species). In addition, four mite species and Rumex species (Polygonaceae) and hence has a have been recorded from members of the genus Ambrosia. relatively broad host range (Ishikawa et al., 1999). The majority of herbivores with a known feeding Of the 20 fungal pathogens found associated with niche are leaf feeders (50%), followed by stem miners Ambrosia species in Eurasia (Table S2), most have a (28%), seed feeders (12%) and flower or pollen feeders wide host range and have little impact on the plant in the (9%). field (Kiss et al., 2003). Outbreaks of disease epidemics Numerous fungal pathogens associated with Ambrosia caused by two biotrophic fungal pathogens, Phyllachora species in the native range have a wide host range, either ambrosiae (Berk. & M.A. Curtis) Sacc. and Plasmopara within the Asteraceae or across a number of different halstedii (Farl.) Berl. & De Toni, did affect A. artemisii- plant families. However, some fungal species are similarly folia in Hungary in 1999 and 2002 (Vajna et al., 2000; restricted to the genus Ambrosia, e.g. Septoria ambrosii- Vajna, 2002), but not in other years (Kiss, 2007). A cola Speg. and Passalora ambrosiae (Chupp) Crous & U. newly described species associated with A. artemisiifolia Braun (synonym Cercospora ambrosiae Chupp; see Table in Hungary, Septoria epambrosiae D.F. Farr (Farr & S4). Other pathogen species such as the white blister ÔrustÕ, Castlebury, 2001), is also known from A. trifida in Pustula tragopogonis (Pers.) Thines [synonym Albugo North America. In China, the damaging microcyclic rust tragopogonis (D.C.) Gray], and the true rust P. xanthii Puccinia xanthii Schwein. has been recorded from have been recorded from a number of different genera A. trifida as P. xanthii f. sp. ambrosiae-trifidae Batra within the Asteraceae; however, P. tragopogonis and, (Lu et al., 2004), following BatraÕs initial classification as indicated earlier, P. xanthii have been shown to of a host-specific P. xanthii accession from the same comprise different formae speciales with a highly host plant in North America (Batra, 1981). This rust restricted host range. The existence of formae speciales species is considered to comprise a number of host- is also known for the powdery mildew species Golovino- specific rust populations adapted to specific Asteraceae myces cichoracearum var. chichoracearum (DC.) V.P. hosts (Batra, 1981; Morin et al., 1993; Kiss, 2007; Seier Heluta (synonym Erisyphe cichoracearum DC.), and a et al., 2009). restricted host range of accessions of this pathogen associated with A. artemisiifolia cannot be ruled out (Ellison & Barreto, 2003). Herbivores and pathogens associated with Ambrosia species in their native range Biological control of Ambrosia species Compared with the low number of phytophagous organisms associated with Ambrosia species in their Biological control of Ambrosia species in their introduced range in Eurasia, numerous species are native range known from their native range. A combination of literature surveys, studies of museum collections and Ambrosia artemisiifolia and A. trifida are also noxious field surveys conducted from 1965 onwards has identi- weeds in their native range, in particular in Canada fied as many as 450 species of insects, mites and fungi (Cowbrough, 2006) and in the northern United States associated with Ambrosia species in North and South (USDA-NRCS, 2009), causing allergenic hay fever America (Goeden & Andres, 1999). On individual (Bassett & Crompton, 1975). As the highest densities Ambrosia species, as many as 113 (on Ambrosia psilo- of both species are found in the most densely populated stachya) and 88 (on Ambrosia confertifolia DC) insect part of Canada (southern Ontario and Quebec), species were recorded in Southern California alone the feasibility of the mycoherbicide approach, i.e. the (Goeden & Ricker, 1975, 1976). Many of these species periodic inundative application of high doses of indi- also feed on other genera in the Asteraceae or other genous pathogens over an entire weed population, was families. However, a combined literature and internet studied in both Canada and the USA. Protomyces survey for species potentially specific at the subtribe level gravidus Davis, which attacks A. artemisiifolia, A. trifida, (i.e. associated with Ambrosia species and for which no Xanthium strumarium L. and members of the genus other host plant record has been found outside of the Bidens (tribe Coreopsideae, Asteraceae), was studied in

Ó 2011 The Authors Weed Research Ó 2011 European Weed Research Society Weed Research 6 E Gerber et al. the USA (Cartwright & Templeton, 1988; Table S4). and parasitoids by the end of summer (Teshler et al., The species causes stem gall disease and killed plants 2002). It was therefore suggested to use it in inundative when these were infected systemically. However, the low biological control and to make releases of beetles early rate of infection and lack of virulence when applied as a in the growing season (Teshler et al., 1996). mycoherbicide strongly limited the ability of this organism to control A. artemisiifolia. The project was Classical biological control of Ambrosia species therefore stopped. worldwide A forma specialis of P. tragopogonis has been described from A. artemisiifolia in Canada (Hartmann There is a long history of classical biological control & Watson, 1980; Appendix S1). Attack by P. tragopog- attempts against exotic Ambrosia, mainly A. artemisii- onis can be very damaging and significantly reduces folia, in different parts of the world, including eastern pollen and seed production if systemic infection is Europe (Russia, former Yugoslavia, Georgia, Ukraine), achieved (Hartmann & Watson, 1980), but difficulties in Australia and Asia (China and Kazakhstan). Classical mass producing this white blister ÔrustÕ have so far biological control of Ambrosia species outside the native prevented the pathogen from being produced commer- range started in the former Soviet Union in the 1960s, cially (Teshler et al., 2002). when more than 30 insect species from North America A Phoma sp., recorded on A. artemisiifolia in North were introduced into quarantine (Goeden & Andres, America, was considered as a potential mycoherbicide 1999). In 1969, the release of the noctuid moth candidate (Brie` re et al., 1995). A combination of this Tarachidia candefacta Huebner (Table S3) collected on Phoma sp. and the leaf beetle Ophraella communa LeSage A. artemisiifolia in Canada and California was the first (Coleoptera: Chrysomelidae) had a synergistic effect and intentional introduction of a natural enemy for the resulted in high plant mortality (Teshler et al., 1996). biological control of an invasive exotic plant into Unfortunately, the culture of Phoma sp. lost its virulence Europe (Kovalev, 1971). In 1972, a subspecies of and attempts to revive or re-isolate the species from T. candefacta collected on A. psilostachya (now natural sites failed (Teshler et al., 2002). Two plurivor- Ambrosia coronopifolia Torr. & A. Gray) was also ous pathogens, the soil-borne fungus Rhizoctonia solani released (Kovalev, 1971; Julien & Griffiths, 1998), but J.G. Kuehn and the Gram-negative bacterium Pseudo- so far, T. candefacta has been unsuccessful as a biologi- monas syringae pv. tagetis (Hellmers) Young, Dye & cal control agent (Appendix S1). Wilkie, have also been preliminarily evaluated as In 1978, the leaf beetle Z. suturalis (Table S3) was potential biocontrol agents for a crop management released and quickly established in the North Caucasus strategy against Ambrosia grayi (A. Nelson) Shinners in (Julien & Griffiths, 1998) and has since spread practi- the USA (Sheikh et al., 2001). Under glasshouse condi- cally over the whole area heavily infested by A. artemisii- tions, R. solani was shown to cause significant disease in folia in Russia (Reznik et al., 2007). In the same year, inoculated A. grayi plants seen as an increase in root the species was also released in Kazakhstan, Georgia necrosis and a reduction in plant emergence, as well as and Ukraine, but establishment is only confirmed in in fresh and dry leaf weight (Wheeler et al., 1998). Kazakhstan (Julien & Griffiths, 1998). Zygogramma Pseudomonas syringae pv. tagetis proved to be patho- suturalis was further released in 1985 and again in 1990 genic towards A. grayi causing systemic chlorosis in in former Yugoslavia (now Croatia). At first, the results infected plants during glasshouse trials. Subsequent field obtained with this beetle in Russia were very promising trials conducted in Texas showed the bacterium to be (Reznik, 1991). It reached densities as high as 5000 effective against the weed at relatively low concentrations individuals per m2 in a crop field in southern Russia and and following a single application (Sheikh et al., 2001). completely destroyed all of the A. artemisiifolia, thereby The beetles Zygogramma suturalis Fabricius (Table increasing crop yield by two- to threefold (Goeden & S3) and Ophraella communa LeSage are natural enemies Andres, 1999). Further investigations have, however, of A. artemisiifolia in Canada and the United States and shown that Z. suturalis is not able to control the were studied as inundative biological control agents weed sufficiently (Reznik, 1991; Reznik et al., 2007; (Teshler et al., 2002). The reduction or cessation of Appendix S1). Z. suturalis oviposition on extensively damaged plants Between 1980 and 1984, three biological control (as observed in the former USSR; Appendix S1) and agents from Me´ xico were introduced into Australia for pupation in soil are, however, an important limitation the biological control of Parthenium hysterophorus L., a for the mass-rearing of this species (Teshler et al., 2002). species closely related to the genus Ambrosia: the Under natural conditions, population densities and leaf-feeding chrysomelid beetle Zygogramma bicolorata impact of O. communa in North America tend to be Pallister, the sap-sucking bug Stobaera concinna (Sta˚ l) low, presumably because of strong attack by predators and the tip-galling moth Epiblema strenuana Walker

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(Table S3; McFadyen & Weggler-Beaton, 2000). All sufficiently specific and ⁄ or damaging, particularly with three insects also attack A. artemisiifolia, and in partic- regard to long-term and sustainable control. The appar- ular, E. strenuana is reported to reduce the size, abun- ent lack of a regular re-occurrence of epiphytotics by dance and pollen production of the weed. In 1990, P. ambrosiae and P. halstedii (Kiss, 2007) raises the Z. suturalis was introduced into Australia from the USA question whether they could be facilitated through to increase A. artemisiifolia control, but the species artificial inundative application of these two fungal failed to establish (Julien & Griffiths, 1998). Presently, pathogens. However, neither of these fungi can be A. artemisiifolia is considered under good control in cultured in vitro; thus, their biology makes them south-eastern Queensland and northern New South presently unsuitable for mass production and application Wales (Palmer et al., 2010). From an economic point as a mycoherbicide. This renders a system management of view (Page & Lacey, 2006), biological control of approach or an inundative application of European A. artemisiifolia is regarded as an outstanding success in antagonists to control A. artemisiifolia in Europe Australia (Palmer et al., 2010). unlikely and leaves either classical biological control or Releases of Z. suturalis in China in 1985, both from an inundative application of exotic organisms for man- Canada and from the former Soviet Union, resulted in aging A. artemisiifolia in Europe by biological means. establishment in some locations, but failed in others When developing a biological control approach as (Wan et al., 1995). The seed-feeding fly Euaresta bella part of an integrated management programme against (Loew) was introduced into China in the late 1980s, but A. artemisiifolia in Europe, priority should be given to as in Russia, this fly failed to establish (Zhou et al., organisms with a narrow host range and that have the 2009). In 1991, E. strenuana was introduced from Aus- potential to either negatively impact the population tralia into China where additional host specificity tests growth rate of ragweed or to reduce ragweed biomass were conducted (Wan et al., 1995). In contrast to results quickly. In terms of host specificity, one of the most from tests conducted in Australia (McFadyen, 1992), critical issues is the close relatedness of the target to the E. strenuana was able to complete its development on a commercially important sunflower, Helianthus annuus. local sunflower variety tested (Wan et al., 1995), but the As sunflower varieties might differ in their susceptibility risk of E. strenuana causing economic damage to sun- to biological control candidates (Morin et al., 1993), flowers was considered to be low (Appendix S1). several varieties need to be included in biosafety In addition to the deliberate releases of these biologi- studies, especially those that occur in the regions where cal control agents, the North American leaf beetle A. artemisiifolia is abundant and biological control O. communa was accidentally introduced into Japan in agents are planned to be released. Only one plant the late 1990s (Yamanaka et al., 2007 and references species of the subtribe Ambrosiinae is considered native therein). In 2001, it was also found in Jiangsu province to Europe, A. maritima, which is furthermore restricted in China (Zhang et al., 2005), from where good control to the Mediterranean. Such a low number of very closely of A. artemisiifolia populations is reported (Zhou et al., related native species increases the chance of finding 2009). Recently, a mass-rearing programme was estab- ÔsafeÕ biological control agents (Pemberton, 2000). On lished with O. communa in China with the aim to use the other hand, because of the observed high within- this agent for inundative application in severely invaded population variation of A. artemisiifolia found in France habitats (Zhou et al., 2009). (Genton et al., 2005), biological control agents should also be not too (genotype or host strain) specific to account for genetic differences among populations and Biological control options for Europe: to control all individuals in a population. learning from the past In terms of impact, flower-, pollen- and seed-feeding While both the inundative and the system management organisms or those that contribute to a reduction in seed approach are primarily aimed at crop weeds, the classical output should be considered first when applying the approach has traditionally and most successfully been classical biological control approach. This is because used against invasive plants spreading over large areas of pollen production is the prime factor causing the high natural and semi-natural habitats, extensively managed impact on human health and a reduction in seed output agro-ecosystems or aquatic ecosystems (environmental is likely to translate into reduced population densities weeds; Mu¨ ller-Scha¨ rer & Schaffner, 2008). As outlined and dispersal of annuals (Ramula et al., 2008). On the earlier, with the possible exception of distinct virulent other hand, natural enemies that quickly reduce strains of Puccinia xanthii as well as the two pathogens the biomass are expected to be especially suited for Phyllachora ambrosiae and Plasmopara halstedii, no an inundative application to reduce crop losses because natural enemy recorded on A. artemisiifolia and other of competition (Mu¨ ller-Scha¨ rer et al., 2000; Harrison exotic Ambrosia species in Eurasia so far appears to be et al., 2001). There is generally a lack of information on

Ó 2011 The Authors Weed Research Ó 2011 European Weed Research Society Weed Research 8 E Gerber et al. whether ragweed specialists are able to reduce biomass pollen load in the air. The third species, Z. disrupta, of A. artemisiifolia quickly, but indirect evidence may occupies a similar feeding niche as Z. suturalis. Addi- come from congeners that are known to damage their tional efforts to establish this species could be considered, host plants. Building on the information compiled in case Z. disrupta does not display oviposition inhibi- earlier, we propose an outline to tackle biological tion on damaged A. artemisiifolia as seen for Z. suturalis. control of A. artemisiifolia in Europe, involving both We rank all these three species as first-priority control pathogens and insects and different biological control agents (Table 1, Fig. 1). strategies for different habitats. Our prioritisation of potential biological control candidates for A. artemisii- Reconsider species that have been studied but, for folia is based on evidence of their narrow host range, different reasons, were never released their feeding niche and control efficacy, availability and suitability to rear, and past experience. This allowed us Zygogramma tortuosa Rogers, originally recorded from to identify 23 potential agents, seven of which were given Ambrosia eriocentra Gray, was introduced for testing in first priority (Table 1 and Fig. 1). quarantine in Russia, but was rejected because adults also fed on sunflower (reviewed in Goeden & Ricker, 1979). Goeden and Ricker (1979) found, however, that Redistribute insects already established as biological Z. tortuosa did not feed and females did not oviposit on control agents in eastern Europe sunflower in open field tests. Furthermore, first instar The moth Tarachidia candefacta is well established in larvae transferred onto sunflowers were not able to Russia but so far is considered an ineffective agent. complete their development. Zygogramma tortuosa might Predation of the exposed larvae (Goeden & Andres, 1999) therefore be reconsidered as a biological control agent, in and unsuitable climatic conditions (Poltavsky & Artok- particular if it does not show a similar oviposition hin, 2006) have been stated as potential reasons for its inhibition on damaged A. artemisiifolia as Z. suturalis. failure. While in the past, strong frosts might have limited Of the three Zygogramma species listed in Table 1, we population growth, Poltavsky and Artokhin (2006) consider Z. disrupta as the most promising biological observed increased numbers in Rostov-on-Don from control candidate and give Z. tortuosa second priority. 2003 onwards after a series of mild winters. Based on the Three cecidomyid flies, Contarinia partheniicola criteria listed above, we give this species first priority for Cockerell and Rhopalomyia ambrosiae Gagne´ and the further studies (Table 1, Fig. 1). Prior to considering stem-mining Neolasioptera ambrosiae Felt (Table S3), are T. candefacta or any other insect tested in Russia for likely to be host specific and have therefore been further relocation or for release in Europe, additional host proposed as potential biological control agents against specificity tests need to be conducted, in particular with A. artemisiifolia (Gagne´ , 1975). Another gall midge, native plant species in the family Asteraceae. At the time Asphondylia ambrosiae Gagne´ , was originally considered when these insects were released in Russia, the main for field release in Australia, but as its larvae feed on emphasis of host specificity tests was placed on crop symbiotic fungi, a release of Asphondylia ambrosiae plants, assuring that the species would not attack culti- would require the simultaneous importation of the fungi, vated species. which makes the use of this cecidomyiid fly as a biological control agent rather unlikely (Goeden & Palmer, 1995). Neolasioptera larvae may also rely on symbiotic fungi, Re-evaluate insect species tested and released in but C. partheniicola and Rhopalomyia ambrosiae are not Russia that failed to establish considered to live in symbiosis with fungi (Skuhrava´ , Three insect species, i.e. Euaresta bella, Trigonorhinus pers. com.). However, these appear to be difficult to tomentosus (Say) and Zygogramma disrupta Rogers, were collect; despite repeated, intensive surveys in Texas and found to be sufficiently specific in host specificity tests Florida, Rhopalomyia ambrosiae could not be relocated conducted in Russia and were released, but did not and only small numbers of C. partheniicola were found establish (Julien & Griffiths, 1998). Additional releases of (Goeden & Palmer, 1995). Nevertheless, these Dipteran these insects should be attempted, in particular to species may have some potential as biological control establish Trigonorhinus tomentosus and E. bella, as these agents against A. artemisiifolia in Europe (Table 1). species occupy feeding niches exploited neither by native herbivores nor by the two established biological control Assessment of additional phytophagous organisms agents T. candefacta and Z. suturalis in Russia. Larvae recorded on Ambrosia species in the native range of E. bella develop in seeds, thereby directly reducing seed output. Trigonorhinus tomentosus feeds as adult and The list of organisms recorded from Ambrosia species in larva on pollen and could directly contribute to reduce their native range is long, and several species appear to

Ó 2011 The Authors Weed Research Ó 2011 European Weed Research Society Weed Research Biological control of Ambrosia in Europe 9

Table 1 Host range, prioritisation and management approach for proposed biological control candidates against Ambrosia artemisiifolia in Europe (see text for details)

Host range* Experimental Priority Management Taxon Field observations studies Biosafety ⁄ feasibility for Europe approach

Insecta Coleoptera Ophraella slobodkini AMBEL AMBEL, Ivafr 1 Classical ⁄ inundative? Smicronyx perpusillus AMBEL ? 1 Classical Smicronyx tesselatus AMBEL, Ambrosia ? Attack of 2 Classical Ambrosia maritima? Trigonorhinus tomentosus Ambca, FRSCO, AMBELà Attack of A. maritima? 1 Classical Ambce, AMBDU, Establishment? AMBER Zygogramma bicolorata§ AMBEL, Parthenium ? Attack of A. maritima? 2 Classical Zygogramma disrupta AMBEL AMBELà Establishment? 1 Classical Zygogramma tortuosa AMBER Ambrosia Attack of A. maritima? 2 Classical Diptera Callachna gibba AMBEL, AMBPS ? Attack of A. maritima? 2 Classical Contarinia partheniicola Ambca, FRSCO, ? Rare in native range? 2 Classical AMBDU, AMBER, AMBPS, Parin Euaresta bella AMBEL AMBELà Establishment? 1 Classical Euaresta toba AMBEL, AMBCU, ? Attack of A. maritima? 2 Classical AMBTE Rhopalomyia ambrosiae AMBEL, AMBPS ? Rare in native range? 2 Classical Hemiptera Stobaera concinna§ AMBEL, Parthenium ? Attack of A. maritima? 2 Classical Lepidoptera Adania ambrosiae FRSAC, AMBEL, ? Attack of A. maritima? 2 Classical Ambca, AMBER, AMBPS Bucculatrix agnella AMBEL ? Attack of A. maritima? 2 Classical Schinia rivulosa AMBEL, AMBPS, ? Attack of A. maritima? 2 Classical Ambrosia Tarachidia candefacta AMBEL, FRSCO, AMBEL– Attack of A. maritima? 1 Classical AMBPS Tischeria ambrosiaeella AMBEL, AMBTE ? Attack of A. maritima? 2 Classical Fungi Ascomycota Dothideomycetes Capnodiales Mycosphaerellaceae Septoria ambrosiicola Speg. Ambrosia Attack of A. maritima? 2 Classical ⁄ inundative? Septoria epambrosiae D.F. Farr Ambrosia Attack of A. maritima? 2 Classical ⁄ inundative? Passalora ambrosiae (Chupp) Ambrosia Attack of A. maritima? 2 Classical Crous & U. Braun Passalora trifidae (Chupp) Ambrosia Attack of A. maritima? 2 Classical U. Braun & Crous Basidiomycota Pucciniomycetes Pucciniales Pucciniaceae Puccinia xanthii Schwein. 1 Classical

*Plant species: EPPO (Bayer) codes used when available (codes in capitals; see http://eppt.eppo.org/index.php); (A. = Ambrosia) FRSAC: A. acanthicarpa; AMBEL: A. artemisiifolia; Ambca: A. chamissonis; FRSCO: A. confertiflora; Ambce: A. chenopodiifolia; AMBCU: A. cumanensis; AMBDU: A. dumosa; AMBDE: A. deltoideae; AMBER: A. eriocentra; AMBPS: A. psilostachya (now A. coronopifolia); AMBTE: A. tenuifolia; Ivafr: Iva frutescens; Parin: Parthenium incanum. Tested as classical biological control agent against A. artemisiifolia. §Released as classical biological control agent against Parthenium hysterophorus. àAccording to tests conducted in Russia but no access to data. –According to tests conducted in Russia (Kovalev, 1971).

Ó 2011 The Authors Weed Research Ó 2011 European Weed Research Society Weed Research 10 E Gerber et al.

Pollen feeder Seed feeder

Col: Trigonorhinus tomentosus Dip: Euaresta bella Seed feeder Defoliator

Col: Smicronyx perpusillus Col.: Zygogramma disrupta Defoliator Defoliator

Col: Ophraella slobodkini Lep: Tarachidia candefacta Leaf pathogen Fig. 1 Most promising candidate species for biological control of Ambrosia artemisiifolia in Europe and their feeding niche. Col., Coleoptera; Dip., Diptera; Bas: Puccinia xanthii Lep., Lepidoptera; Bas., Basidiomycota. have a narrow host range and are potentially of interest Australia for the biological control of P. hysterophorus for biological control (Tables S3 and S4). However, (McFadyen, 1992). Ophraella slobodkini is described only Goeden and Palmer (1995) cautioned that the know- from A. artemisiifolia, but could also be reared on the ledge of the host range information on insects associated closely related Iva frutescens L. in the laboratory with Ambrosiinae might not prove to be reliable. Based (Futuyma, 1991). Larval survival was, however, lower on our prioritisation criteria given earlier, we propose and development time longer than on A. artemisiifolia, several species associated with A. artemisiifolia in its suggesting that this species is indeed more specific than native range to be considered as potential biocontrol O. communa that was accidentally introduced to China agents for A. artemisiifolia (Table 1, Fig. 1) or poten- and Japan (Appendix S1). Provided O. slobodkini is as tially any of the other invasive Ambrosia species in damaging as its congener, it might contribute to the Europe (Table S1). control of A. artemisiifolia in Europe, using either the classical or the inundative approach (as with Evaluation of invertebrates O. communa in China). We therefore give this species The high number of species in the Curculionidae genus first priority. Previous experiences in biological control Smicronyx and the Lepidoptera genera Schinia, Buccul- of A. artemisiifolia indicate that defoliators can be atrix and Epiblema recorded from Ambrosia species effective in controlling plant populations in the invaded (Table S3) may indicate that speciation has occurred range (Appendix S1). within the Ambrosiinae and consequently, narrow host In addition to these three species that seem to feed associations can be expected. Furthermore, species in exclusively on A. artemisiifolia under field conditions, the genera Epiblema and Smicronyx have been reported several other insect species are reported from A. artemisii- to be successful biological control agents against folia and also from other Ambrosia species in their Parthenium hysterophorus (McFadyen & Weggler-Beaton, native range (Table 1). These species could possibly be 2000), indicating their potential as biological control considered as biological control agents against agents for Ambrosia species. Of particular interest is the A. artemisiifolia in Europe, if the risk of non-target seed-feeding weevil, Smicronyx perpusillus Casey, which attack on A. maritima, the only native congeneric is only reported from A. artemisiifolia and to which we species in Europe, turns out to be minimal. Moreover, therefore give first priority (Table 1, Fig. 1). several insect and mite species listed in Table S3, Two additional species with a presumably narrow including the eriophyid mite Eriophyes boycei Keifer, host range are the moth Bucculatrix agnella Clemens and which was also considered as a potential agent of the leaf beetle Ophraella slobodkini Futuyma, both of A. artemisiifolia in the former Soviet Union but did which feed on leaves. A closely related species of not survive the transport (Goeden et al., 1974), have Bucculatrix agnella, Bucculatrix parthenica Bradley, been recorded on other Ambrosia species, but not on was found to be specific enough to be released in A. artemisiifolia under field conditions. Some of these

Ó 2011 The Authors Weed Research Ó 2011 European Weed Research Society Weed Research Biological control of Ambrosia in Europe 11 herbivores may also have potential as biological control Cercospora ambrosiae) and Passalora trifidae (Chupp) agents against A. artemisiifolia, provided that this plant U. Braun & Crous (synonym Cercospora trifidae Chupp species belongs to their fundamental host range. 1949), is restricted to the genus Ambrosia (Table S4). These fungal pathogens could be considered for bio- Evaluation of fungal pathogens logical control, if the risk of damage to A. maritima, the The potential of pathogens to impact adversely on only European native congeneric species, was assessed A. artemisiifolia and its pollen production was docu- as minimal. Based on this uncertainty, as well as a lack mented during naturally occurring epiphytotics of of data about the impact of the two Septoria and Phyllachora ambrosiae and P. halstedii observed in Passalora species on their Ambrosia hosts in the native Hungary in 1999 and 2002 (Vajna et al., 2000; Vajna, range, we give them second priority. However, Septoria 2002; Kiss et al., 2003). as well as Cercospora species have previously been Among the range of fungal pathogens known to evaluated and used against a number of invasive weed attack Ambrosia species in their native range (see species and, in the case of Septoria passiflorae, applied Table S4), the highly damaging rust fungus P. xanthii inundatively to control banana poka vine, Passiflora is the most promising candidate for biological control of tripartita var. tripartia, in Hawaii (Julien & Griffiths, A. artemisiifolia. The rust completes its life cycle on one 1998). of the host species, and while recorded from numerous genera of the Asteraceae (Hennen et al., 2005), individ- New surveys in source regions matching specific ual rust populations or accessions within P. xanthii have European conditions shown a high degree of host specialisation. For example, an accession of P. xanthii collected on A. trifida in We expect that further explorations of the natural North America showed high specificity to its original enemy complexes associated with A. artemisiifolia or host, but failed to infect A. artemisiifolia and closely related species will reveal new candidate species, X. strumarium; this accession was therefore named or biotypes of known species (Tables S3 and S4), for the P. xanthii f. sp. ambrosiae-trifidae (Batra, 1981). Simi- biological control of A. artemisiifolia in Europe. larly, accessions of the rust originating from Xanthium Most biological control agents for A. artemisiifolia species were shown to be non-infectious to A. artemisii- and A. trifida have so far been collected in the eastern folia (Morin et al., 1993; Kiss, 2007). Accessions of United States and Canada, where both ragweed species P. xanthii from A. artemisiifolia collected in Texas occur. However, the genus Ambrosia covers a much (USA) in 1989 showed evidence of an equally high host larger geographical area, including different climatic specialisation; they proved to be highly pathogenic to an zones. Targeting regions with climatic conditions com- A. artemisiifolia biotype from Australia during initial parable to those in the invaded range in Europe evaluations, while failing to infect P. hysterophorus and increases the chances that biological control agents will Xanthium species (H.C. Evans, pers. comm.). The establish and persist. The richest source of natural significant impact P. xanthii can have on its hosts has enemies is probably the Sonoran desert region (i.e. in the been documented in China when a sudden outbreak of south-western United States and northern Me´ xico), the P. xanthii f. sp. ambrosiae-trifidae on A. trifida caused centre of origin and diversification of the genus Ambro- serious die-back of infected plants in 2003 (Lu et al., sia (Harris & Piper, 1970). Surveys for phytophagous or 2004). In Australia, a strain of P. xanthii successfully pathogenic organisms in the Sonoran Desert have so far controlled a number of highly invasive Xanthium species mainly been restricted to the state of California, and of the Noogoora burr complex (Morin et al., 1996). large areas remain unexplored (Goeden & Palmer, Based on the documented host specificity of individual 1995). Natural enemies from the Sonoran desert itself P. xanthii accessions and their damaging impact, we give might well be pre-adapted to warmer climates in this rust first priority. Doubts have been cast on the Mediterranean Europe, e.g. the Rhone Valley, Northern potential of P. xanthii as a biocontrol agent for Italy and some parts of the Balkans. These organisms A. artemisiifolia, based on a lack of disease incidence are, however, unlikely to become adapted to more following unsuccessful attempts to collect the rust on temperate or continental areas, except if they are this host in North America in 2002 and 2003. However, collected at high elevations. The most likely regions to these latest surveys included neither the region in Texas, harbour cold-adapted specialised herbivore species are where the most recent collections of this rust strain were the mountains of Me´ xico adjacent to the Sonoran desert made, nor the majority of other sites where previous (Harris & Piper, 1970) and ⁄ or areas at higher elevation herbarium material had been collected (Kiss, 2007). in the northern part of Me´ xico (Bohar & Vajna, 1996). The documented host range of S. ambrosiicola and Because of their eco-geographical separation from the S. epambrosiae, as well as of P. ambrosiae (synonym southern parts of the United States through the Sonoran

Ó 2011 The Authors Weed Research Ó 2011 European Weed Research Society Weed Research 12 E Gerber et al. desert, different organisms are likely to have evolved in with A. artemisiifolia in its native range are likely to have these mountain ranges. a very narrow host range that is restricted either to the Early on in the history of biological control of target species itself or to a few species within the genus Ambrosia species, mountain regions of South America Ambrosia. Altogether, we identified 18 insect and 5 were also highlighted as a potential source for climat- fungal pathogens to be promising candidates for a ically adapted phytophagous species for Canada and classical biological control approach, and of these, we Europe (Harris & Piper, 1970). These regions are likely prioritised six insect and one fungal pathogen species to have different natural enemy complexes because they (Table 1, Fig. 1). Second, an inundative approach will be are isolated from the Mexican mountain range by a necessary for crop fields that suffer from ragweed tropical region. The presence of several Ambrosia species infestations. Candidate biological control agents for in mountain regions of South America originates from mass-rearing and repeated releases against ragweed in an early phylogenetic invasion, indicating that the genus Europe are the defoliator O. slobodkini or the fungus might have been present there long enough to acquire S. epambrosiae (Table 1). A combination of biological specialist phytophages originating from the local fauna agents with other weed management tools will probably (Harris & Piper, 1970). Despite these recommendations be needed to produce acceptable levels of overall weed by Harris and Piper (1970), few surveys have been control in crops (Mu¨ ller-Scha¨ rer et al., 2000). conducted and little information is available on species associated with Ambrosia in South America. In 1975– Acknowledgements 1976, McFadyen (1976) conducted limited surveys on insects associated with A. tenuifolia (later attributed to We thank Paul Hatcher and two anonymous reviewers Ambrosia elatior, an accepted synonym of A. artemisii- for comments on an earlier version of this manuscript. folia) in northern Argentina and reported several The study was partially funded by the National Centre potentially specific insect species from this area. Besides of Competence in Research (NCCR) Plant Survival, the an undescribed Liothrips species (Appendix S1), two research programme of the Swiss National Science stem-mining beetles (Curculionidae and Cerambycidae) Foundation and the University of Fribourg (Poˆ le de were sent to a quarantine facility in Canada, but the Recherche). We also thank Monica Miller (Tarachidia species entered diapause from which they failed to candefacta), Dan Bahauddin (Smicronyx), Margarether emerge and no host specificity tests could be conducted Brummermann (Trigonorhinus tomentosus), Thomas (Maw, 1981). The weevil Conotrachelus albocinereus Whelan (http://www.whelanphoto.com; Euaresta bella), Fiedler (Coleoptera, Curculionidae), which was col- Mike Quinn (TexasEnto.net; Zygogramma disrupta) and lected from A. elatior in Argentina, was released in Doug Futuyma (Ophraella slobodkini) for allowing us to Australia as a biological control agent of Parthenium use their photographs or hand-drawings. hysterophorus and has proven to be highly damaging to this weed (R. McFadyen, pers. comm.). Recent collec- References tions in warm temperate, mountainous areas of south- ern Brazil have revealed new pathogen records on ARMESTO JJ & PICKETT STA (1985) Experiments on distur- A. artemisiifolia (H.C. 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