BioControl (2018) 63:333–347 https://doi.org/10.1007/s10526-017-9844-6 Weed biological control in the European Union: from serendipity to strategy . . . . Richard H. Shaw Carol A. Ellison Helia Marchante Corin F. Pratt . . Urs Schaffner Rene F. H. Sforza Vicente Deltoro Received: 31 March 2017 / Accepted: 17 September 2017 / Published online: 20 October 2017 The Author(s) 2017. This article is an open access publication Abstract Biological control of weeds is a globally Chrysomelidae), against common ragweed, Ambrosia recognised approach to the management of some of artemisiifolia L. (Asteraceae), which are providing the most troublesome invasive plants in the world. beneﬁts to an increasing number of Member States of Accidental introductions of agents accounted for all the European Union. Recent programmes involving weed biological control agent establishments in the the intentional introduction of biological control European Union until 2010, but these examples agents against target weeds including Fallopia japon- include some current or emerging control successes ica (Hout.) Ronse Decr. (Polygonaceae), Impatiens both large and small, from the redistribution of the glandulifera Royle (Balsaminaceae) and Acacia weevil Stenopelmus ruﬁnasus Gyllenhal (Coleoptera: longifolia (Andrews) Willd (Fabaceae) show a shift Curculionidae) for the control of small outbreaks of from luck to judgement in the European Union. The Azolla ﬁliculoides Lam. (Azollaceae), to the large inclusion of new weed targets on the European scale control provided by the cochineal insect Dacty- Invasive Species Regulation should lead to a growth lopius opuntiae (Cockerell) (Hemiptera: Dactylopi- in the proﬁle and use of biological control which idae), used against some problematic prickly pears would be assisted by the publication of any successes (Opuntia spp. (Cactaceae)), and the ragweed beetle from the few intentional introductions covered in this Ophraella communa LeSage (Coleoptera: paper. Keywords Regulation Fallopia japonica Handling Editors: Mark Schwarzla ¨nder, Cliff Moran Ambrosia artemisiifolia Opuntia ﬁcus-indica Azolla and S. Raghu. R. H. Shaw (&) C. A. Ellison C. F. Pratt U. Schaffner CABI Europe-UK, Bakeham Lane, Engleﬁeld Green, CABI Europe-Switzerland, Rue des Grillons 1, Egham, Surrey TW20 9TY, UK 2800 Delemont, Switzerland e-mail: firstname.lastname@example.org R. F. H. Sforza H. Marchante USDA-ARS-European Biological Control Laboratory, Coimbra College of Agriculture, Polytechnic of Coimbra, Campus International de Baillarguet, 810, Avenue du Bencanta, 3045-601 Coimbra, Portugal Campus Agropolis, 34980 Montferrier-sur-Lez, France V. Deltoro H. Marchante VAERSA-Generalitat Valenciana, Avinguda Corts Department of Life Sciences, Centre for Functional Valencianes 20, 46015 Valencia, Spain Ecology, University of Coimbra, 3000-456 Coimbra, Portugal 123 334 R. H. Shaw et al. ﬁliculoides Impatiens glandulifera Acacia into the USA in 1999 to control saltcedar (De Loach longifolia et al. 2003), but turned out to be a group of ﬁve sibling species with different geographical origins ranging from the Mediterranean region to Asia (Tracy and Robbins 2009). Fortunately, all ﬁve chrysomelid Introduction species defoliate saltcedar populations in the south- eastern USA and contributed to the successful control Biological control of weeds is a recognised and widely of these widespread invasive trees. It is also possible that an agent may arrive from a neighbouring country applied tool in several regions of the world (Clewley et al. 2012; Suckling and Sforza 2014), but the where it has been released. The ﬂy U. quadrifasciata European Union (EU) is a noticeable exception was ofﬁcially released in Canada against varied (Sheppard et al. 2006). This is surprising considering knapweed (Asteraceae) targets, and was found across the extensive use of biological control agents (BCAs) the border in Montana, Oregon and Washington, USA in glasshouses (Minks et al. 1998; Eilenberg et al. in seed heads of spotted knapweed, Centaurea stoebe 2000), for which Europe is a leading region and the use L. (Story 1984). It is now considered to be widespread of at least 176 species of exotic arthropods that have in more than 50% of its plant host’s invasive range in not been conﬁned in glasshouses but released, against Canada and the USA. Furthermore, it is possible that pests of agriculture, across Europe (Gerber et al. an agent may arrive through accidental transportation 2016). The reasons for this are manifold and have been from its native range: the weevil, Larinus carlinae Olivier (formerly L. planus) (Coleoptera: Curculion- discussed by Sheppard et al. (2006) and Shaw et al. (2011) but a prime issue appears to remain the general idae), that feeds on seed heads of Cirsium arvense (L.) ignorance of the potential of classical biological Scop. (Asteraceae) was accidentally introduced into control of weeds amongst policy makers, which is the USA from Europe (Wheeler and Whitehead 1985). exacerbated by their risk aversion mind-set. The Of the 19 species of weed BCAs believed to have purpose of this account is to document selected been released accidentally in North America, 17 are examples of weed biological control to illustrate the credited with having a signiﬁcant impact on their long history of its inadvertent practice in Europe and respective ‘‘target’’ weeds. Only two, L. carlinae and then to highlight its recent (since 2010) intentional and Cactoblastis cactorum (Berg) (Lepidoptera: Pyrali- dae) have had adverse effects (Suckling and Sforza successful implementation. 2014). The weevil L. carlinae found on C. arvense in Beneﬁcial but accidental introductions of weed the 1960s may be useful for controlling seed produc- biological control agents in the EU tion to prevent large areas of infestation from expanding further (Drlik et al. 2000). However, it Accidental introductions of phytophagous arthropods has been shown to attack a congeneric native thistle, against invasive weeds are not uncommon and it is Cirsium undulatum var. tracyi (Rydb.) S.L.Welsh, in often difﬁcult to trace the origin of such introductions. Colorado (Louda and O’Brien 2002). The most They may be revealed during agent redistribution such publicised and notorious case occurred when C. as the ﬁrst discovery in North America of Urophora cactorum arrived in Florida in 1989 from the quadrifasciata (Weigen) (Diptera: Tephritidae) on Caribbean islands where it had been released to spotted knapweed, accidentally redistributed in seed control invasive Opuntia species (Cactaceae) (Zim- heads believed to only contain the ofﬁcially approved mermann et al. 2001). Upon colonizing Florida, and more recently Mexico, it has started feeding on native Urophora afﬁnis, or because of post-release evalua- tion studies on ofﬁcially released BCAs, such as the Opuntia species and is considered by many as a case of Diorhabda beetles (Coleoptera: Chrysomeli- serious failure of biological control safety. It is dae) on saltcedar, Tamarix species (Tamaricaceae), important to note that such unintentional introductions which involved the misidentiﬁcation of the agents. have been relatively rare (Suckling and Sforza 2014). The latter case of Diorhabda elongata (Brulle)is Some unintended arrivals have been shown to have particularly interesting as this taxon was introduced impressive positive impacts and the EU has been in receipt of such species, all of which have been 123 Weed biological control in the European Union: from serendipity to strategy 335 intentionally applied elsewhere in the world against neighbouring plants at mean distances of 80–100 cm their target weeds, as is documented below. occurred after four weeks. After 16 months, healthy colonies were found up to 2 km away from the Opuntia ﬁcus-indica (L.) Mill. (prickly pear) introduction site. The resulting damage apparent after (Cactaceae) six months was mild chlorosis, but this translated to the loss of up to 50% of cladodes as well as the loss of The prickly pear cactus, Opuntia ﬁcus-indica,is a turgor just four months later. Furthermore, the well-known perennial succulent widely planted as a cochineal attack induced a marked decline in the fruit and fodder crop, but which has also become a plant’s sexual reproduction, since the outer cladodes problematic invader around the world. It has become of newly infested prickly pears were the ﬁrst to invasive in Spain, particularly in areas of high collapse, leaving mainly ligniﬁed stems or old clado- disturbance, near urban areas and abandoned ﬁelds des without fruit production (V. Deltoro, unpublished (Vila ` et al. 2003; Padro ´ n et al. 2011) but also in natural data). Similar results from South Africa were areas where it competes with native vegetation and described by Paterson et al. (2011) for O. stricta severely modiﬁes habitats and landscapes. One of its infested with D. opuntiae. natural enemies, Dactylopius opuntiae (Cockerell) Observations suggest a gradient of cochineal-dam- (Hemiptera: Dactylopiidae), is a sap-sucking insect, age moving from high in the southernmost provinces commonly known as a cochineal. Nine species are of the Valencia region where plants are killed, to less known from the Americas (De Lotto 1974; Guerra damage in more northerly areas, where the plants are 1991) and ﬁve have been reported from Mexico still able to produce new cladodes. It is unclear (Chavez-Moreno et al. 2009). All of them feed on cacti whether this is due to the differing period of residence (Mann 1969; De Lotto 1974) and exhibit marked host of the insect or the humidity gradient. It is important to speciﬁcity. For instance, at least two biotypes of D. report that no non-target feeding has been observed opuntiae exist, each with a restricted host range: the despite intentional attempts to infect other Opuntia stricta biotype feeds on low growing Opuntia stricta species in the ﬁeld (V. Deltoro, unpublished data), as (Haw.) Haw. whereas the ﬁcus biotype is associated expected given the well-established host speciﬁcity of with tree-like O. ﬁcus-indica (Githure et al. 1999; cactus-feeding Dactylopius species (Mann 1969;De Volchansky et al. 1999). Lotto 1974; Githure et al. 1999; Volchansky et al. Dactylopius species are now distributed across 1999). several regions of the world due to intentional The fact that D. opuntiae can be found across a wide introductions aimed at starting up a pigment industry area covering the whole Spanish Mediterranean arc (Lounsbury 1915) or controlling infestations of dif- suggests the insect is well adapted to the regional ferent Opuntia species (Zimmermann and Moran climate. Based on experiences in other dry and warm 1991; Hosking et al. 1994; Foxcroft and Hoffmann regions of the world where cochineal insect species 2000; Klein 2002). However, D. opuntiae has also have been released successfully (Lounsbury 1915; spread, presumably accidentally, to Israel (Spodek Zimmermann 1981; Zimmermann and Moran 1991; et al. 2014) and Spain by unknown routes. In the latter Hosking 1984), it is likely that long distance dispersal country, it was ﬁrst recorded in Hellın (Murcia) in of the cactus will be limited, due to the collapse of the 2007 (Llorens Climent 2009), from where it expanded outer, fruit-producing cladodes, and this should be rapidly along the coastal Mediterranean areas of followed by a gradual decline in the density of Spain, tracking the almost continuous distribution of established prickly pear populations and eventually its introduced host plant O. ﬁcus-indica (Sanz Elorza local extinctions. Thus, this unintentional introduction et al. 2004; Serrano-Montes et al. 2016). Dispersal offers the only realistic opportunity to limit the rates of the insect and any injury to the cactus host expansion of an invasive plant capable of displacing have been recorded following the intentional infesta- and preventing the regeneration of native vegetation in tion of prickly pear populations with D. opuntiae- dry areas of Spain (Gimeno and Vila ` 2002; Sanz laden cactus cladodes (V. Deltoro, unpublished data). Elorza et al. 2004). Nevertheless, the collapse of O. The results show that dispersal on infested plants took ﬁcus-indica populations has also raised some concern place 15 days after inoculation and spread to in southern Spanish regions, since the plant is 123 336 R. H. Shaw et al. appreciated by some as a component of Mediterranean EU-COST Action SMARTER (‘Sustainable manage- landscapes, despite its negligible economic impor- ment of Ambrosia artemisiifolia in Europe’) was tance as a crop (Serrano-Montes et al. 2016). In clear launched in 2012. Emphasis was put on biological contrast, the Autonomous Government of Catalonia control by promoting and coordinating studies on the has taken advantage of the opportunity that the host-speciﬁcity and impact of selected insect and cochineal insects provide for O. ﬁcus-indica control, fungal BCAs (Gerber et al. 2011). In 2013, biological and has deliberately introduced them to the Medas control efforts against common ragweed experienced archipelago Natural Park, to control this troublesome an unexpected boost when the North American leaf colonizer. beetle Ophraella communa LeSage (Coleoptera: Chrysomelidae) was detected in Northern Italy and Ambrosia artemisiifolia L. (common ragweed) Southern Switzerland (Bosio et al. 2014;Mu ¨ ller- (Asteraceae) Scha ¨rer et al. 2014). The beetle was ﬁrst reported close to the international airport of Milano, suggesting that Common ragweed is an annual or short-lived peren- this species was accidentally introduced, a situation nial plant that is native to North America. This species reminiscent of the arrival and detection of Trichapion has invaded several regions of the world, including lativentre (Beguin-Billecocq) (Coleoptera: Api- Europe, western and eastern Asia, South Africa, onidae), at Durban International Airport, South Africa Australia and New Zealand (Essl et al. 2015). In (Hoffmann and Moran 1991). Ophraella communa Europe, it was introduced with seed imports from was not prioritized in the SMARTER project, because North America in the 19th century. Today, A. host speciﬁcity tests under laboratory conditions had artemisiifolia is particularly abundant in the Pannon- shown that O. communa can complete its life-cycle on ian plain, northern Italy and south-eastern France (Essl sunﬂower, Helianthus annuus L. (Asteraceae) (Palmer et al. 2015). Common ragweed is notorious for its and Goeden 1991). impact on human health, due to its highly allergenic Interestingly, O. communa had already been pollen, but it is also increasingly becoming a major accidentally introduced to another area outside of weed in agriculture. In Europe, the current costs its native range, i.e. to Japan (Moriya and Shiyake associated with common ragweed impacts on farming 2001). Since its ﬁrst detection in Japan in the 1990s and human health are estimated to be of the order of it rapidly expanded its distribution over the main approximately 4.5 billions € per year (Bullock et al. Japanese islands of Honshu, Shikoku, and Kyushu 2012). (Moriya and Shiyake 2001). From Japan, it spread Since the 1960s, biological control had been to Korea (Sohn et al. 2002) and to China. In China, considered as a management option against common it was ﬁrst found in the east (Jiangsu province) in ragweed in different parts of the world, including non- 2001 (Meng and Li 2005), from where it continued EU Member States in Europe (Gerber et al. 2011). The spreading to provinces in southern China (Zhou noctuid moth Tarachidia candefacta (Hu ¨ bner) (Lepi- et al. 2010). Field studies in China showed, doptera: Noctuidae), which was released in Russia in however, that the risk of O. communa causing 1969, was the ﬁrst such intentional attempt to control signiﬁcant damage to sunﬂower plants in the ﬁeld is common ragweed by biological means (Kovalev low (Cao et al. 2011; Zhou et al. 2011). Today, O. 1971), but so far with little impact. In the 1970s and communa and the deliberately introduced moth 1980s, the leaf beetle Zygogramma suturalis (Fabri- Epiblema strenuana Walker (Lepidoptera: Tortrici- cius) (Coleoptera: Chrysomelidae) was released in dae) are mass-reared and actively distributed in Russia, Georgia, Ukraine and the former Yugoslavia China for the biological control of common ragweed (now Croatia) (Julien and Grifﬁths 1998). First results (Zhou et al. Zhou et al. 2014). The history of obtained with this BCA were promising (Reznik accidental introductions and rapid dispersal by O. 1991), but more recent investigations suggest that Z. communa highlights the need for concerted actions suturalis is not able to offer effective control of by authorities of all European countries in which O. common ragweed (Reznik et al. 2007). communa can establish permanently. To advance the development of sustainable man- As soon as O. communa was detected in the EU, agement strategies for A. artemisiifolia in Europe, the laboratory and open ﬁeld host speciﬁcity and impact 123 Weed biological control in the European Union: from serendipity to strategy 337 studies were taken up as part of SMARTER to assess The impacts of A. ﬁliculoides in South Africa, the risks and beneﬁts related to the accidental estab- following its introduction as an ornamental in 1947, lishment of this beetle. In the ﬁrst year of its detection, became so signiﬁcant that a classical biological O. communa reached high enough densities to com- control programme was initiated against the plant in pletely defoliate and prevent ﬂowering and seed set of the mid-1990s. Native range surveys in North America most ragweed plants in the Milan area. Bonini et al. followed by host range testing resulted in the selection (2016) showed that airborne common ragweed pollen and release of the frond-feeding weevil Stenopel- levels observed in the Milan area in 2013 and 2014 mus ruﬁnasus Gyllenhal (Coleoptera: Curculionidae) were approximately 80% lower than in years prior to in 1997 (McConnachie et al. 2003). Stenopelmus the establishment of O. communa. The decrease in ruﬁnasus is an Azolla specialist, with A. ﬁliculoides ambrosia pollen observed in the Milan area could not and A. caroliniana Willd serving as host plants in the be explained by meteorology in these years, suggest- weevil’s native range (Madeira et al. 2013; Pemberton ing that the decrease is related to the presence of large and Bodle 2009). The biological control programme numbers of O. communa (Bonini et al. 2016). Studies proved incredibly successful, with the weevil reducing are also underway to assess the non-target risks posed the A. ﬁliculoides population to a level at which it was by O. communa to sunﬂower and native plant species. no longer considered a problem within three years, Because of the potentially signiﬁcant positive impact with an estimated beneﬁt:cost ratio of 15:1 by 2010 of O. communa on health costs, the French Ministries anticipated in a post-release evaluation (McConnachie of Health, Agriculture and the Environment mandated et al. 2003). an expert appraisal to assess the efﬁcacy of O. Europe has beneﬁtted from the unintentional communa as a BCA against common ragweed in introduction of S. ruﬁnasus, probably as a stow- France (ANSES 2017). In the ﬁnal document, it was away on A. ﬁliculoides which was widely sold, suggested that the beneﬁts of an establishment of O. until quite recently. The weevil was ﬁrst reported in communa to France could be signiﬁcant, but that France in 1901 (Bedel 1901) and was detected in further host speciﬁcity studies with native plant the Netherlands and in the United Kingdom (UK) species are warranted (ANSES 2017). in the early part of the century (Florencio et al. 2015; Janson 1921). Stenopelmus ruﬁnasus is now Azolla ﬁliculoides Lam (water fern) (Azollaceae) widespread and can also be found in Belgium, Germany, Ireland, Spain, Ukraine, Italy and Portu- The Azolla water fern is native to the Americas but has gal in association with A. ﬁliculoides (Carrapic ¸o become naturalised on most continents worldwide et al. 2011; Florencio et al. 2015). Naturalised (Lumpkin and Plucknet 1980). In parts of its intro- weevil populations can have a dramatic impact on duced range, A. ﬁliculoides is utilised commonly as a A. ﬁliculoides infestations, but S. ruﬁnasus has been green manure for rice and other crops in certain areas found to be a less effective BCA in Europe than in of Asia due to its ability to ﬁx atmospheric nitrogen, South Africa (Gassmann et al. 2006). It is possible and as fodder for livestock. In much of its introduced that differences in the climatic conditions, particu- range, however, A. ﬁliculoides is a highly invasive larly between northern Europe and South Africa, weed that can double its biomass in less than a week could play a signiﬁcant role in limiting the impacts (Arora and Singh 2003) to form dense ﬂoating mats of the weevil on A. ﬁliculoides, with fewer across freshwater bodies. The impacts of A. ﬁlicu- generations per year, induced diapause and potential loides are numerous and include: reduction in dis- mortality over winter and limited dispersal on solved oxygen in the water body and decreased light cooler days year-round. Richerson and Grigarick penetration through the mat, negatively affecting (1967) estimated that S. ruﬁnasus would complete submerged ﬂora and fauna; direct impediment to 4–6 generations per year in part of its native range, leisure activities such as angling and boating; threat to California, whereas Hill (1998) estimated up to ten livestock and people when mistaken for solid land; generations per year would be possible in South impediment to water ﬂow; clogging of pipes, pumps Africa. Parts of southern Europe may be better and ﬂoodgates (Gratwicke and Marshall 2001; Hill suited to S. ruﬁnasus and could expect good levels and Cilliers 1999; Janes et al. 1996). of A. ﬁliculoides control during the summer months 123 338 R. H. Shaw et al. Pteridium aquilinum (L.) Kuhn where the weevil is established. This has been observed in the Valencia region (East Spain) where (Dennstaedtiaceae) a precipitous fall in the extent of A. ﬁliculoides infestations occurred upon arrival of the weevil in Strategic weed biological control in the EU can be considered to have begun in earnest in the 1980s with a 2011. In the UK, where widespread control of this weed is less consistent, S. ruﬁnasus is being mass- project targeting bracken fern, P. aquilinum, for the UK. This project was successful in that highly speciﬁc reared by the Centre for Agriculture and Bio- sciences International (CABI) for redistribution. natural enemies from South Africa were identiﬁed. The Department for Environment, Food & Rural However, these agents were never released because Affairs (Defra) classiﬁes the weevil, which has the UK authorities requested a prohibitively expensive been present in the UK for close to a century, as quarantine ﬁeld cage to be built to further conﬁrm the agents’ speciﬁcity. Nowadays this project would ‘‘ordinarily resident’’, so there are no restrictions to its redistribution in England and Wales. During the probably not be commissioned because some of the fundamental requirements for successful classical summer months, the weevil is shipped across the region to be applied to A. ﬁliculoides outbreaks, weed biological control are not met: the target weed is cosmopolitan, even though its agents are not; and proving to be a highly effective agent, commonly resulting in local eradication of the weed (C. Pratt, bracken has been credited with providing a habitat for rare and protected lepidopteran species (Pakeman and unpublished data). Following on from this work, and with similar results, S. ruﬁnasus mass rearing Marrs 1993). and releases have been trialled in the Netherlands and Belgium, along with ﬁeld assessments of Heracleum mantegazzianum Sommier & Levier naturalised populations under the EU-funded (Apiaceae) RINSE (Reducing the Impact of Non-native Species in Europe) programme. An implementation plan, developed between 2002 and 2005 under an EU-funded project entitled ‘Giant Alien’, for the biological control of Heracleum mantegazzianum (among other common names known The strategic use of weed biological control agents in the EU as giant hogweed), was an integral part of subsequent research efforts for the sustainable control of this alien Altica carduorum Gue ´rin-Me ´neville (Coleoptera: weed in Europe. The aim was to evaluate current Chrysomelidae) European guidelines for the importation of exotic organisms. However, no suitably speciﬁc agents were In 1969, small-scale caged and uncaged ﬁeld studies in found during the project which could have been taken forward through a pest risk assessment for potential the UK on the leaf beetle, A. carduorum, a natural enemy of Cirsium arvense (Asteraceae) from France, future release (Cock and Seier 2007). effectively became the ﬁrst release of a classical weed BCA in an EU Member State (Baker et al. 1972). In Fallopia japonica var japonica (Hout.) R. Decr. (Japanese knotweed) (Polygonaceae) this case the researchers set out to determine whether Altica carduorum appeared capable of establishment Japanese knotweed is one of the worst weeds in in Great Britain. The results were similar to those from Canada (Peschken et al. 1970), in that there was no Europe and certainly the worst invasive plant in Great successful survival over winter. It is not clear what Britain from an economic standpoint, as it costs that authorisation, if any, was secured or what host range country £165 million each year (Williams et al. 2011), testing was carried out on the beetle prior to this work mainly borne by land developers and homeowners. The threat to property posed by Japanese knotweed is in the UK. This type of activity would be highly restricted today but the fact that both the source considered so great that many banks restrict lending for house purchases if it is found on or near the country and the release country are both members of the EU means that those restrictions would be national property and sellers are legally obliged to report its presence to prospective buyers. As a rhizomatous rather than regional. 123 Weed biological control in the European Union: from serendipity to strategy 339 perennial plant, which is largely clonal and with no UK in each of those years and the fact that releases real conﬂicts of interests identiﬁed, this was a highly took place on just one occasion each season on small attractive target for biological control. It was, there- isolated patches of knotweed. In 2015, further psyllids fore, the subject of the ﬁrst ofﬁcially sanctioned were re-collected from the same locality in Japan as release, in 2010, of a WBA in the EU: namely the those in the quarantine culture and are currently Japanese knotweed psyllid Aphalara itadori Shinji undergoing ﬁeld assessment, having been reared in the (Hemiptera: Psyllidae). This was the culmination of a lab for several generations. The strategy is to start research programme which began in the year 2000 future release cultures from those newly sourced with an initial scoping study funded by the USDA adults that successfully survive the winter in the ﬁeld Forest Service and the then Welsh Development in the UK, so as to select for the hardier individuals. Agency and continued in earnest from 2003, supported Releases will also take place on multiple occasions by a consortium of funders. throughout the season with overlapping generations, The psyllid A. itadori was found to be the best and at riparian sites with large knotweed populations, potential agent of the 186 insect species and more than using various stages of psyllids on potted plants. This 40 fungal species found attacking the plant in Japan approach should increase the chances of successful (Shaw et al. 2009) and was selected to be petitioned for establishment and spread. release in England and Wales in 2009. Once it was Acacia longifolia (Andrews) Willd (long-leaved agreed that licensing should be done under Plant Health Regulations, a Pest Risk Analysis (PRA) was wattle) (Fabaceae) produced which received comments from a wide range of interested parties before being reviewed by the Acacia longifolia is a small tree or shrub, native to Advisory Committee on Releases to the Environment south-eastern Australia, which is invasive in Portugal, (ACRE). Further questions were raised by the latter South Africa and other regions of the globe (Sanz committee regarding possible secondary, tertiary and Elorza et al. 2004). In Portugal, A. longifolia invades community level impacts of the release of the psyllid extensive areas of coastal ecosystems and is replacing which were addressed by further quarantine studies. native plant communities previously dominated by The data package was then subjected to a scientiﬁc herbs and small shrubs and creating monospeciﬁc peer review by three anonymous experts, prior to woody stands (Marchante et al. 2015). In addition, it becoming part of a public consultation. Once no changes soil chemistry and functioning (Marchante further substantive issues emerged, Ministerial et al. 2008), and the ecological networks of associated approval was sought and subsequently granted for communities (Lo ´ pez-Nu ´ n ˜ ez et al. 2017). The invasion restricted release at a limited number of sites. For the by this species also reduces forest productivity, mainly ﬁrst time in weed biological control history, the in littoral pine plantations, with consequent negative release had an eradication plan attached, should economic impacts. The extensive production of long- anything go wrong. Though this process appears lived seeds is a key characteristic that contributes extreme (and is completely impractical) when com- signiﬁcantly to the dispersal ability and invasiveness pared with other more experienced biological control- of A. longifolia (Marchante et al. 2010). utilising nations, it should be borne in mind that this The ﬁrst intentional release of a BCA against this was a pioneering activity for Europe and a very weed in Europe occurred in November 2015 when cautious approach was justiﬁed. Trichilogaster acaciaelongifoliae (Froggatt) (Hy- The psyllid did not perform well in UK conditions, menoptera: Pteromalidae), a host-speciﬁc Australian during the restricted ﬁve year release programme bud-galling wasp, was permitted for use in Portugal. (2010–2015), and despite proving itself capable of The female wasps lay their eggs on ﬂower buds (and overwintering successfully, populations either failed later also on vegetative buds) inducing the formation to establish or did not ﬂourish. This could be due to the of galls, instead of ﬂowers, which reduces seed founder population having been reared under contin- production and curbs the growth of A. longifolia. ual Japanese summer conditions in a growth room for The bud-galling wasp is univoltine (one generation per almost 90 generations, but could also be due to year) and most of the annual life cycle is spent as eggs, abnormal and unseasonal weather experienced in the larvae and pupae within the developing galls. The 123 340 R. H. Shaw et al. authorization to release T. acaciaelongifoliae in data) showing successful establishment. A second Portugal took 12 years and included host-speciﬁcity release campaign (still with galls imported from South testing involving 40 plant species (Marchante et al. Africa) took place in November–December 2016, and 2011), several analyses and risk assessments by further ﬁeld releases are planned (with South African or national (both conservation and phytosanitary author- Portuguese galls depending on the rate of establishment ities) and European (Standing Committee on Plant in Portugal) until the agent is established and wide- Health SCOPH, from European Commission and spread in Portugal. European Food Safety Authority EFSA) entities (more The long process that led to the release of T. details in Shaw et al. 2016). Following their positive acaciaelongifoliae has paved the way for new biolog- opinion (EFSA PLF Panel 2015a) EFSA went on to ical control projects. Host speciﬁcity testing on two make a statement with constructive observations and Melanterius species (Coleoptera: Curculionidae) tar- recommendations on the process of assessing risk geting other invasive Acacia species in Portugal, has (EFSA PLH Panel 2015b). been authorized. This was via a much faster process The collaborative research and release process was under the National Authorities ICNF, Portuguese carried out by the Centre for Functional Ecology Institute for Nature Conservation and Forests, and (University of Coimbra) and Coimbra College of DGAV, the Portuguese National Authority for Animal Agriculture (Polytechnic Institute of Coimbra) and Health, Phytosanitation and Food Safety, and will begin in 2017. beneﬁted greatly from the extensive experience from researchers from the Department of Biological Sciences, University of Cape Town, South Africa Impatiens glandulifera Royle (Himalayan balsam) where the BCA T. acaciaelongifoliae has been used (Balsaminaceae) successfully for more than 30 years (Dennill 1990). Galls of the BCA, despite being native to Australia, Following the release of the psyllid for the biological were obtained from South Africa, for both host control of Japanese knotweed in the UK, a second speciﬁcity testing and ﬁeld releases. Only females were invasive weed was targeted for biological control in released due to the wasp’s parthenogenetic reproduc- that country, Impatiens glandulifera. This annual plant tion and, despite the challenge of overcoming asyn- was introduced to the UK in 1839 as a garden chrony between the phenology of the wasps (from the ornamental. Since then, it has spread by seed, both southern hemisphere) and target plants (in the northern naturally and with human assistance, over much of the hemisphere), the ﬁrst records of establishment are UK and other parts of Europe (Beerling and Perrins encouraging. After the ﬁrst releases (in November 1993). Himalayan balsam can tolerate a wide range of 2015) at eight locations mostly along the Portuguese environmental conditions, enabling the plant to coast, by July–August 2016, adult females emerged rapidly form dense monocultures on wasteland, from galls at half the sites indicating the completion of woodland, railways lines and particularly in riparian the wasp’s life cycle for the ﬁrst time in the wild in the habitats. As well as directly reducing biodiversity northern hemisphere (Marchante et al. 2017). The life (Hulme and Bremner 2006), especially amongst cycle took approximately 8–9 months to complete, invertebrate communities (Tanner et al. 2013), instead of taking the expected one year after oviposi- Himalayan balsam also lures pollinators away from tion, as happens in the southern hemisphere, so the native plants, decreasing the ﬁtness of native species prospects are good for successive generations of the (Chittka and Schu ¨ rkens 2001). River banks are laid BCA to fully synchronise their life cycles to northern bare by the weed after it dies back in the winter, which hemisphere seasons and with the phenology of the host renders them more prone to erosion (Greenwood and plant. The second-generation galls resulting from Kuhn 2014). Himalayan balsam was considered to be a oviposition by wasps emergent in July–August 2016 good target as it is a ﬂeshy annual plant with an in Portugal were ﬁrst observed in February 2017 at apparently limited number of introductions to Europe. some of the sites, indicating that they may also complete At the time, this latter factor was expected to mean that the cycle in less than one year: by May 2017 a one (or a few) strains of the rust that was utilized as a signiﬁcant increase in the number of mature galls was BCA would be able to infect all populations of the observed on those sites (H. Marchante, unpublished weed in Europe, due to the host’s limited genetic 123 Weed biological control in the European Union: from serendipity to strategy 341 variability. It was also recognised that to control the The UK Minister for the Environment approved extensive riparian populations of this annual weed release on the 27th July 2014, making this the ﬁrst using traditional physical and chemical methods fungal BCA to be released against a weed in the EU. would need the coordination of the multiple land Since then, the rust has been released at 25 sites across owners on a catchment scale, which is unlikely to be England and southern Wales and readily spread onto realised. naturalised Himalayan balsam, reaching signiﬁcant The search for natural enemies started in 2006 with levels of infection at some sites. The rust was also surveys undertaken throughout the native range of the found to complete its life cycle under UK climatic Himalayan foothills from Pakistan to Nepal. A range of conditions. However, ﬁeld observation and inocula- insects and fungal plant pathogens were collected, but tion studies showed variation in the susceptibility of most of the insects were found to feed on a broad set of different plant populations to the Indian rust strain, Impatiens species. A rust fungus, Puccinia komarovii suggesting that the plant could have been introduced var. glanduliferae (Uredinales), was observed to infect on more than one occasion into the UK and Europe Himalayan balsam throughout the areas surveyed, (Nagy and Korpelainen 2015). This could mean that causing signiﬁcant damage to infected plants both at the rust will only be effective against a subset of the the seedling stage (stem infection, usually leading to Himalayan balsam populations in the UK, dependent plant death) and to leaves of the remaining maturing on their origin. Additionally, it has highlighted the potential need to release additional strains of the rust plants and, hence, was prioritised for further study (Tanner et al. 2014). An isolate of the rust fungus in order to have impact on other plant genetic forms of collected in the Kullu Valley, Himachal Pradesh, India the target plant in its invasive range (Varia et al. 2016). was selected and screened for speciﬁcity against 74 plant A new strain of the rust from Pakistan (previously species and an additional ten varieties of three widely collected and stored in liquid nitrogen at CABI) has grown ornamental species in the UK (Tanner et al. 2015). now been checked for safety by testing it on the most Only I. glandulifera and Impatiens balsamina L. (a non- closely related plant species to Himalayan balsam and, native ornamental species with very low commercial as expected, has the same level of speciﬁcity as the value) were fully susceptible to the rust. Indian strain. Initial screening suggests that the strain The licensing procedure that was followed for the can heavily infect some populations of the plant that Japanese knotweed psyllid (as recorded above) was are not signiﬁcantly infected by the Indian strain. replicated for the rust including the submission of a Permission to release the new rust strain from PRA to UK regulators, followed by a public consul- quarantine was granted by Defra in early 2017 after tation. However, the process then differed as microor- internal consultation concerning any risk posed by the ganisms are not regulated by the UK Wildlife and new strain. A molecular analysis of UK and native- Countryside Act 1981. In this case the SCOPH, which range populations of Himalayan balsam is underway had only been informed prior to the release of the at CABI to ascertain how many genetic types there are psyllid rather than consulted, took an interest in the in the country and if necessary to help target future proposal for release and withheld their endorsement of surveys to collect new rust strains in the native range. the PRA. The committee signalled its intention to pass Further development of this tool, speciﬁcally targeting the application to the EFSA for further assessment as the genes governing plant resistance/susceptibility to the PRA only considered the UK as the intended area of the rust could also allow site-speciﬁc assessment of introduction and requested the UK Defra Minister to likely success and inform other countries of the delay issuing a licence for the release of the rust from susceptibility of their invasive balsam populations to quarantine. This was an understandable position this promising biological control agent. because with rusts there can be no eradication plan once they are released into the wild since spores cannot be contained and could potentially cross the Channel Discussion into Europe carried on wind currents. In response, the PRA was redrafted to include data relevant to the new Historically, Europe has, and still is beneﬁting from the area of introduction, the whole of Europe, after which unplanned spread of some weed biological control SCOPH endorsed the release of the rust. agents. Although mostly successful, these serendipitous 123 342 R. H. Shaw et al. cases of biological control carry the risk of encouraging eriophyid mite (Acari: Eriophyidae) is a highly future illegal and inadequately researched releases and promising candidate agent (S. Varia, unpublished are clearly not procedurally or ethically correct, nor data). Some terrestrial species such as Solanum safe. The positive outcomes of such releases have elaeagnifolium Cavanilles (Solanaceae) and Ailanthus served an inadvertent purpose in that people in Europe altissima (Mill.) Swingle (Simaroubaceae) are also are becoming more aware of the potential of natural potential targets for biological control in Europe. enemies to control large scale weed invasions. In The EU is moving from a period of serendipity to a parallel, more and more research towards intentional period of strategy regarding weed biological control releases in the EU is being undertaken as the result of and this should be to the beneﬁt of the economies and strategic national funding. It is expected that the environments in those Member States affected by the European Invasive Species Regulation (1143/2014) worst invasive plants. More non-native species are will further beneﬁt this discipline since promising being regulated than ever before and the regulatory biological control target species are included on the pathways for the licensing of exotic weed biological initial list of 37 species published by the EU Commis- control agents have been made clear by recent projects sion in its implementing regulation 2016/1141, for that have culminated in the release of agents from which Member States are obliged to publish a manage- multiple taxa within the EU. There is no shortage of ment plan. There are now 23 plants on this list, after its target weeds and ten of the species highlighted in the reviews by Gassmann et al. (2006) and Sheppard et al. recent expansion, and the scale of some of these invasions leave few alternatives to biological control. (2006) are included as species of European concern in For example, Spain cannot continue indeﬁnitely the recent EU Regulation on Invasive Species and spending tens of millions of Euros (Anonymous 2010) more are likely to be added at each revision of the list. on the mechanical removal of water hyacinth (Eich- In the section of the regulation covering the manage- hornia crassipes (Mart.) Solms) (Pontederiaceae) ment of invasive species that are widely spread, there from the Guadiana river. The favoured BCA, a weevil is a requirement for Member States to have in place (Neochetina eichhorniae Warner) (Coleoptera: Cur- effective management measures within 18 months of culionidae), should be able to establish and control the their inclusion on the list, and that these measures weed as it has done on many occasions elsewhere in should be proportionate and prioritised based on a risk ecoclimatic ranges that are similar to those of the evaluation and their cost effectiveness. Though that Mediterranean basin. In addition, the invasion of timescale is too short for a candidate biological control Ludwigia spp. (Onagraceae) in France has such agent to be developed, adopting a proactive strategy is signiﬁcant environmental and economic impacts over likely the best approach as some of the targets in such a large area (Muller 2004) that land managers question have previously proven BCAs available. often give up management attempts. Work is in In Europe, at present, weed biological control is progress in Argentina where potential BCAs have very much a concern at the national level and there is a already been identiﬁed such as Liothrips ludwigi lack of coordination when it comes to any regional Zamar et al. (Thysanoptera: Phlaeothripidae) (Zamar work. Research is currently carried out by teams on et al. 2013), and an as yet unidentiﬁed Puccinia rust behalf of their host nations in some countries that have (C. Ellison, unpublished data). Furthermore, there is the necessary quarantine facilities and experience to ongoing research into the potential for biological do the work safely, such as the UK, Portugal, Ireland, control of Hydrocotyle ranunculoides L.f. (Apiaceae) Switzerland, France and, to some extent, Italy and (Cabrera-Walsh et al. 2013) which is invasive in both Greece. A sensible next step would be for work to the UK and the Netherlands, as well as of La- commence on those species highlighted above with garosiphon major (Ridley) Moss (Hydrocharitaceae) the affected countries sharing the costs and conducting where an ephydrid ﬂy (Diptera: Ephydridae) may have the research in collaboration with experienced potential as a BCA (Mangan and Baars 2013). In research groups that have established quarantine addition to those species on the EU list, there are other facilities. Going forward, one key need in any aquatic and riparian weeds for which there is ongoing collective EU or European strategy would be the biological control research, including Crassula helm- application of a prioritisation tool, such as that sii (T. Kirk) Cockayne (Crassulaceae), for which an developed by Paynter et al. (2009) which would allow 123 Weed biological control in the European Union: from serendipity to strategy 343 Forest Service before being picked up by a consortium of fun- any resources secured as a result of the regulation on ders adding Defra, Network Rail, Environment Agency, South invasive species, to be expended on the most appro- West Regional Development Agency, British Waterways (now priate and important weeds in the EU and in the rest of Canals and Rivers Trust), all coordinated by Cornwall Council. Europe. At present, however, the biggest challenge is It is now funded mainly by Defra with support from the Welsh Assembly Government and AAFC. ensuring that classical weed biological control is given due consideration by decision makers who are inher- Open Access This article is distributed under the terms of the ently risk averse or unaware of the technique. The Creative Commons Attribution 4.0 International License (http:// biological control community in Europe needs to creativecommons.org/licenses/by/4.0/), which permits unre- stricted use, distribution, and reproduction in any medium, continue to engage in raising awareness so that provided you give appropriate credit to the original classical biological control can gain the conﬁdence author(s) and the source, provide a link to the Creative Com- of regulators and politicians in Europe as well as some mons license, and indicate if changes were made. of their advisors in the ecology and conservation communities who may lack the necessary balance to consider relative risk of the agent and that of its target weed (Downey and Paterson 2016). Classical biolog- References ical control is a highly successful, cost-effective and Anonymous (2010) Cuadernos del Guadiana no. 4 Confederacio ´ n environmentally sound management strategy to Hidrogra ´ﬁca del Guadiana. http://www.chguadiana.es/corps/ deploy against weeds, as it has been for well over a chguadiana/data/resources/revista_digital/ﬁle/cuadernosdelgua- century in many other non-EU countries across the diana4_diciembre2010.pdf world and is currently under-utilised. ANSES (2017) Efﬁcacite ´ du cole ´opte `re Ophraella communa utilise ´ comme agent de lutte biologique contres les ambroisies et e ´valuation des e ´ventuels risques associe ´s. Acknowledgements Many sincere thanks are given to the Anses (Agence nationale de se ´curite ´ sanitaire de l’ali- reviewers and in particular the special edition editorial team for mentation, de l’environnement et du travail), Maisons- providing such thorough reviews and guidance which have Alfort, 96 pp resulted in a much improved paper. For the prickly pear- ´ Arora A, Singh PK (2003) Comparison of biomass productivity Dactylopius monitoring we are grateful to Patricia Perez Rovira, ´ ´ and nitrogen ﬁxing potential of Azolla spp. Biomass Cristobal Torres Rodenas, Miguel Angel Gomez Serrano, Jose ´ ´ Bioenerg 24:175–178 Miguel Aguilar Serrano, Valentın Tena Lazaro and the Natura- ´ Baker CRB, Blackman RL, Claridge MF (1972) Studies on 2000 squads of Castellon, for their involvement and help Haltica carduorum Guerin (Coleoptera: Chrysomelidae) throughout the process. For the common ragweed project support is acknowledged from EU COST Action FA1203 an alien beetle released in Britain as a contribution to the ‘‘Sustainable management of Ambrosia artemisiifolia in Europe biological control of creeping thistle, Cirsium arvense (L.) (SMARTER)’’ (http://internationalragweedsociety.org/ Scop. J Appl Ecol 9:819–830 smarter). The Acacia research (from 2003 to 2016) was sup- Bedel L (1901) Description et moeurs d’un nouveau genre de ported by Portuguese Foundation for Science and Technology curculionides de France. Bull Soc Entomol Fr 6:358–359 (FCT) and European funds POCI/POCTI/COMPETE/FEDER, Beerling DJ, Perrins JM (1993) Biological ﬂora of the British through projects INVADER (POCTI/BSE/42335/2001), Isles. Impatiens glandulifera Royle (Impatiens roylei INVADER-II (POCi/AMB/61387/2004), INVADER-B Walp). J Ecol 81:367–382 (PTDC/AAG-REC/4607/2012) and INVADER-IV (PTDC/ Bonini M, Sikoparija B, Prentovic M, Cislaghi G, Colombo P, ¨ ¨ AAG:REC/4896/2014). Lo ´ pez-Nu ´ n ˜ ez FA, Freitas H, Hoff- Testoni C, Grewling Ł, Lommen STE, Muller-Scharer H, Smith M (2016) A follow-up study examining airborne mann JH, Impson F, Marchante E are acknowledge by their Ambrosia pollen in the Milan area in 2014 in relation to the signiﬁcant contribution along several parts of the all process. accidental introduction of the ragweed leaf beetle A. Torrinha, S. Ribeiro, N. Ce ´sar de Sa ´, I. Seic ¸a, O. Ferreira, J. Ophraella communa. Aerobiologia 32:371–374 Carlos Filipe, C. O’Connor, S. Quaresma, C. Gonc ¸alves, K. Dix, Bosio G, Massobrio V, Chersi C, Scavarda G, Clark S (2014) L. Barrico, R. Miranda, P. Duarte, R. Euse ´bio, A. Soﬁa Nunes Spread of the ragweed leaf beetle, Ophraella communa and R. Vaz are acknowledged for help in ﬁeld and laboratory LeSage, 1986 (Coleoptera Chrysomelidae), in Piedmont work. For the Himalayan balsam research work thanks are given Region (Northwestern Italy). Boll Soc Entomol Ital to Rob Tanner, Harry Evans, Sonal Varia, Kate Pollard and 146:17–30 Marion Seier. Many donors have provided resources to this Bullock J, Chapman D, Schaffer S, Roy D, Girardello M, project with the main funding from Defra, Natural Resources Haynes T, Beal S, Wheeler B, Dickie I, Phang Z, Tinch R Wales and Natural England. We are also very grateful to par- (2012) Assessing and controlling the spread and the effects ticipating local action groups, River Trusts, Water Boards, the of common ragweed in Europe (ENV B2/ETU/2010/0037). Environment Agency and local authorities that have provided European Commission, Final Report invaluable support with the rust release programme. The knot- Cabrera-Walsh G, Maestro M, Magalı ´ Dalto Y, Shaw R, Seier weed project was ﬁrst funded by the Welsh Development M, Cortat G, Djeddour D (2013) Persistence of ﬂoating Agency (now Welsh Assembly Government) and the USDA 123 344 R. H. Shaw et al. pennywort patches (Hydrocotyle ranunculoides, Arali- Petitpierre B, Richter R, Schaffner U, Smith M, Starﬁnger aceae) in a canal in its native temperate range: effect of its U, Vautard R, Vogl G, von der Lippe M, Follak S (2015) natural enemies. Aquat Bot 110:78–83 Biological ﬂora of the British Isles: Ambrosia artemisi- Cao Z, Wang H, Meng L, Li B (2011) Risk to non-target plants ifolia. J Ecol 104:1069–1098 from Ophraella communa (Coleoptera: Chrysomelidae), a Florencio M, Ferna ´ndez-Zamudio R, Bilton DT, Dı ´az-Paniagua potential biological control agent of alien invasive weed C (2015) The exotic weevil Stenopelmus ruﬁnasus Gyl- Ambrosia artemisiifolia (Asteraceae) in China. Jpn Soc lenhal, 1835 (Coleoptera: Curculionid) across a ‘‘host- Appl Entom Zool 46:375–381 free’’ pond network. Limnetica 34:79–84 Carrapic ¸o F, Santos R, Serrano A (2011) First occurrence of Foxcroft LC, Hoffmann JH (2000) Dispersal of Dactylopius Stenopelmus ruﬁnasus Gyllenhal, 1835 (Coleoptera: Erir- opuntiae Cockerell (Homoptera: Dactylopiidae), a bio- hinidae) in Portugal. Coleopt Bull 65:436–437 logical control agent of Opuntia stricta (Haworth.) Cha ´vez-Moreno CK, Tecante A, Casas A (2009) The Opuntia Haworth. (Cactaceae) in the Kruger National Park. Koedoe (Cactaceae) and Dactylopius (Hemiptera: Dactylopiidae) 43:1–5 in Mexico: a historical perspective of use, interaction and Gassmann A, Cock MJW, Shaw RH, Evans HC (2006) The distribution. Biodivers Conserv 18:3337–3355 potential for biological control of invasive alien aquatic Chittka L, Schu ¨ rkens S (2001) Successful invasion of a ﬂoral weeds in Europe: a review. Hydrobiologia 570:217–222 market. Nature 411:653 Gerber E, Schaffner U, Gassmann A, Hinz HL, Seier M, Mu ¨ ller- Clewley GD, Eschen R, Shaw RH, Wright DJ (2012) The Scha ¨rer H (2011) Prospects for biological control of Am- effectiveness of classical biological control of invasive brosia artemisiifolia in Europe: learning from the past. plants. J Appl Ecol 49:1287–1295 Weed Res 51:559–573 Cock MJW, Seier MK (2007) The scope for biological control of Gerber E, Mai L, Schaffner U (2016) Review of invertebrate giant hogweed, Heracleum mantegazzianum. In: Pysek P, biological control agents introduced into Europe. CABI, Cock MJW, Nentwig W, Ravn HP (eds) Ecology and Wallingford management of giant hogweed (Heracleum mantegazz- Gimeno I, Vila M (2002) Recruitment of two Opuntia species ianum). CABI, Wallingford, pp 255–271 invading abandoned olive groves. Acta Oecol 23:239–246 De Loach CJ, Lewis PA, Herr JC, Carruthers RI, Tracy JL, Githure GW, Zimmerman HG, Hoffman JH (1999) Host Johnson J (2003) Host speciﬁcity of the leaf beetle, Dior- speciﬁcity of biotypes of Dactylopius opuntiae (Cockerell) habda elongata deserticola (Coleoptera: Chrysomelidae) (Hemiptera: Dactylopiidae): Prospects for biological con- from Asia, a biological control agent for saltcedars (Ta- trol of Opuntia stricta (Haworth) Haworth (Cactaceae) in marix: Tamaricaceae) in the Western United States. Biol Africa. Afr Entomol 7:43–48 Control 27:117–147 Gratwicke B, Marshall BE (2001) The impact of Azolla ﬁlicu- De Lotto G (1974) On the status and identity of the cochineal loides Lam. on animal biodiversity in streams in Zim- insects (Homoptera: Coccoidea: Dactylopiidae). J Entomol babwe. Afr J Ecol 39:216–218 Soc South Afr 37:167–193 Greenwood P, Kuhn NJ (2014) Does the invasive plant, Impa- Dennill GB (1990) The contribution of a successful biocontrol tiens glandulifera, promote soil erosion along the riparian project to the theory of agent selection in weed biocon- zone? An investigation on a small watercourse in northwest trol—the gall wasp Trichilogaster acaciaelongifoliae and Switzerland. J Soils Sediments 14:637–650 the weed Acacia longifolia. Agric Ecosyst Environ Guerra G (1991) Biosystematics of the family Dactylopiidae 31:147–154 (Homoptera: Coccinea) with emphasis on the life cycle of Downey PO, Paterson ID (2016) Encompassing the relative Dactylopius coccus Costa. Doctoral Thesis, Faculty of the non-target risks from agents and their alien plant targets in Virginia Polytechnic Institute and State University, biological control assessments. BioControl 61:615–630 Blacksburg Drlik T, Woo I, Swiadon L, Quarles W (2000) Integrated Hill MP (1998) Life history and laboratory host range of management of Canada thistle. IPM Pract 22:1–9 Stenopelmus ruﬁnasus, a natural enemy for Azolla ﬁlicu- EFSA, PLH Panel (2015a) Risk to plant health in the EU terri- loides in South Africa. BioControl 43:215–224 tory of the intentional release of the bud-galling wasp Hill MP, Cilliers CJ (1999) Azolla ﬁliculoides Lamarck (Pteri- Trichilogaster acaciaelongifoliae for the control of the dophyta: Azollaceae), its status in South Africa and con- invasive alien plant Acacia longifolia. EFSA J trol. Hydrobiologia 415:203–206 13:4079–4127 Hoffmann JH, Moran VC (1991) Biological control of Sesbania EFSA, PLH Panel (2015b) Statement on the assessment of the punicea (Fabaceae) in South Africa. Agric Ecosyst Environ risk posed to plant health in the EU territory by the inten- 37:151–173 tional release of biological control agents of invasive alien Hosking JR (1984) The effect of temperature on the population plant species. EFSA J 13:4134–4146 growth potential of Dactylopius austrinus De Lotto (Ho- Eilenberg J, Enkegaard A, Vestergaard S, Jensen B (2000) moptera: Dactylopiidae), on Opuntia aurantiaca Lindley. Biocontrol of pests on plant crops in Denmark: present Austral Entomol 23:133–139 status and future potential. Biocontrol Sci Techn Hosking JR, Sullivan PR, Welsby SM (1994) Biological control 10:703–716 of Opuntia stricta (Haw.) Haw. var. stricta using Dacty- Essl F, Biro ´ K, Brandes D, Broennimann O, Bullock JM, lopius opuntiae (Cockerell) in an area of New South Wales, Chapman DS, Chauvel B, Dullinger S, Fumanal B, Guisan Australia, where Cactoblastis cactorum (Berg) is not a A, Karrer G, Kazinczi G, Kueffer C, Laitung B, Lavoie C, successful biological control agent. Agric Ecosyst Environ Leitner M, Mang T, Moser D, Mu ¨ ller-Scha ¨rer H, 48:241–255 123 Weed biological control in the European Union: from serendipity to strategy 345 ´ ´ ˜ Hulme P, Bremner ET (2006) Assessing the impact of Impatiens Marchante H, Lopez-Nunez FA, Freitas H, Hoffmann JH, glandulifera on riparian habitats: partitioning diversity Impson F, Marchante E (2017) First report of the estab- components following species removal. J Appl Ecol lishment of the biocontrol agent Trichilogaster acaciae- 43:43–50 longifoliae for control of invasive Acacia longifolia in Janes RA, Eaton JW, Hardwick K (1996) The effects of ﬂoating Portugal. Bull OEPP/EPPO 47:274–278 mats of Azolla ﬁliculoides Lam. and Lemna minuta Kunth McConnachie AJ, De Wit MP, Hill MP, Byrne MJ (2003) on the growth of submerged macrophytes. Hydrobiologia Economic evaluation of the successful biological control of 340:23–26 Azolla ﬁliculoides in South Africa. Biol Control 28:25–32 Janson OE (1921) Stenopelmus ruﬁnasus Gyll., an addition to Meng L, Li BP (2005) Advances on biology and host speciﬁcity the list of British coleoptera. Entomol Mon Mag of the newly introduced beetle, Ophraella communa 57:225–226 LeSage (Coleoptera: Chrysomelidae), attacking Ambrosia Julien MH, Grifﬁths MW (1998) Biological control of weeds: a artemisiifolia (Compositae) in continent of China. Chin J world catalogue of agents and their target weeds, 4th edn. Biol Control 21:65–69 CABI Publishing, Wallingford Minks AK, Blommers LHM, Ramakers PMJ, Theunissen J Klein H (2002) Biological control of invasive cactus species (1998) Fifty years of biological and integrated control in (Family Cactaceae). Cochineal insects (Dactylopius spp). Western Europe: accomplishments and future prospects. PPRI Leaﬂet Series: Weeds Biocontrol No 2.2 In: Proceedings of the 50th international symposium on Kovalev OV (1971) Phytophages of ragweeds (Ambrosia L.) in crop protection, Gent, 5 May 1998. Part I: Mededelingen— North America and their application in biological control in Faculteit Landbouwkundige En Toegepaste Biologische the USSR. Zool Zh 50:199–209 (in Russian) Wetenschappen, Universiteit Gent, vol 63, pp 165–181 Llorens Climent JM (2009) Relacion de nuevas plagas de cul- Moriya S, Shiyake S (2001) Spreading the distribution of an tivos encontradas en Espan ˜ a en los ultimos diez an ˜ os. exotic ragweed beetle, Ophraella communa LeSage. Jpn J Phytoma Esp 212:50–55 Entomol 4:99–102 ´ ´ ´ Lopez-Nun ˜ ez FA, Heleno RH, Ribeiro S, Marchante H, Muller S. (2004) Plantes invasives en France. Museum National Marchante E (2017) Four-trophic level food webs reveal d’Histoire Naturelle, Paris ¨ ¨ the cascading impacts of an invasive plant targeted for Muller-Scharer H, Lommen STE, Rossinelli M, Bonini M, biocontrol. Ecology 98:782–793 Boriani M, Bosio G, Schaffner U (2014) Ophraella com- Louda SM, O’Brien CW (2002) Unexpected ecological effects muna, the ragweed leaf beetle, has successfully landed in of distributing of exotic weevil, Larinus planus (F.), for the Europe: fortunate coincidence or threat? Weed Res biological control of Canada thistle. Conserv Biol 54:109–119 16:717–727 Nagy AM, Korpelainen H (2015) Population genetics of Lounsbury CP (1915) Plant killing insects: the Indian cochineal. Himalayan balsam (Impatiens glandulifera): comparison Agric J S Afr 1:537–543 of native and introduced populations. Plant Ecol Div Lumpkin TA, Plucknet DL (1980) Azolla: Botany, physiology, 8:317–321 and use as a green manure. Econ Bot 34:111–153 Padro ´ n B, Nogales M, Traveset A, Vila ` M, Martı ´nez-Abraı ´nA, Madeira PT, Center TD, Coetzee JA, Pemberton RW, Purcell Padilla DP, Marrero P (2011) Integration of invasive MF, Hill MP (2013) Identity and origins of introduced and Opuntia spp. by native and alien seed dispersers in the native Azolla species in Florida. Aquat Bot 111:9–15 Mediterranean area and the Canary Islands. Biol Invasions Mangan R, Baars JR (2013) Use of life table statistics and 13:831–844 degree day values to predict the colonisation success of Pakeman RJ, Marrs RH (1993) Bracken. Biologist 40:105–109 Hydrellia lagarosiphon Deeming (Diptera: Ephydridae), a Palmer WA, Goeden RD (1991) The host range of Ophraella leaf mining ﬂy of Lagarosiphon major (Ridley) Moss communa Lesage (Coleoptera: Chrysomelidae). Coleopt (Hydrocharitaceae), in Ireland and the rest of Europe. Biol Bull 45:115–120 Control 64:143–151 Paterson ID, Hoffmann JH, Klein H, Mathenge CW, Neser S, Mann J (1969) Cactus feeding insects and mites. Bull US Natl Zimmermann HG (2011) Biological control of Cactaceae Mus 256:1–158 in South Africa. Afr Entomol 19:230–246 Marchante E, Kjøller A, Struwe S, Freitas H (2008) Short and Paynter Q, Hill R, Bellgard S and Dawson M (2009) Improving long-term impacts of Acacia longifolia invasion on the targeting of weed biological control projects in Australia. belowground processes of a Mediterranean coastal dune A report prepared for Land & Water Australia, by Landcare ecosystem. Appl Soil Ecol 40:210–217 Research NZ, Auckland. http://lwa.gov.au/products/ Marchante H, Freitas H, Hoffmann JH (2010) Seed ecology of pn22434 an invasive alien species, Acacia longifolia (Fabaceae), in Pemberton RW, Bodle JM (2009) Native North American Portuguese dune ecosystems. Am J Bot 97(11):1–11 Azolla weevil, Stenopelmus ruﬁnasus (Coleoptera: Cur- Marchante H, Freitas H, Hoffmann JH (2011) Assessing the culionidae), uses the invasive Old World Azolla pinnata as suitability and safety of a well-known bud-galling wasp, a host plant. Fla Entomol 92:153–155 Trichilogaster acaciaelongifoliae, for biological control of Peschken D, Friesen HA, Tonks NV, Banham FL (1970) Acacia longifolia in Portugal. Biol Control 56:193–201 Releases of Altica carduorum (Chrysomelidae: Coleop- Marchante H, Marchante E, Freitas H, Hoffmann JH (2015) tera) against the weed Canada thistle (Cirsium arvense)in Temporal changes in the impacts on plant communities of Canada. Can Entomol 102:264–271 an invasive alien tree, Acacia longifolia. Plant Ecol Reznik SY (1991) The effects of feeding damage in ragweed 216:1481–1498 Ambrosia artemisiifolia (Asteraceae) on populations of 123 346 R. H. Shaw et al. Zygogramma suturalis (Coleoptera, Chrysomelidae). biological control of Himalayan balsam (Impatiens glan- Oecologia 88:204–210 dulifera). Eur J Plant Pathol 141:247–266 Reznik SY, Spasskaya IA, Dolgovskaya, MY, Volkovitsh MG, Tanner RA, Pollard KM, Varia S, Evans HC, Ellison CA (2015) Zaitzev, VF (2007) The ragweed leaf beetle Zygogramma First release of a fungal classical biocontrol agent against suturalis F. (Coleoptera: Chrysomelidae) in Russia: current an invasive alien weed in Europe: biology of the rust, distribution, abundance and implication for biological Puccinia komarovii var. glanduliferae. Plant Pathol control of common ragweed, Ambrosia artemisiifolia L. In: 64:1130–1139 Julien MH, Sforza R, Bon MC, Evans HC, Hatcher PE, Tracy JL, Robbins TO (2009) Taxonomic revision and bio- Hinz HE, Rector BG (eds). XII International Symposium geography of the Tamarix-feeding Diorhabda elongata on Biological Control of Weeds, La Grande Motte, France. (Brulle ´, 1832) species group (Coleoptera: Chrysomelidae: CAB International, Wallingford, pp 614–619 Galerucinae: Galerucini) and analysis of their potential in Richerson PJ, Grigarick AA (1967) The life history of biological control of tamarisk. Zootaxa 2101:1–152 Stenopelmus ruﬁnasus (Coleoptera:Curculionidae). Ann Varia S, Pollard K, Ellison C (2016) Implementing a novel weed Entomol Soc Am 60:351–354 management approach for Himalayan balsam: progress on Sanz Elorza M, Dana Sa ´nchez E, Sobrino Vesperinas E (2004) biological control in the UK. Outlooks Pest Man Atlas de las plantas alo ´ ctonas invasoras en espan ˜ a. Direc- 27(5):198–203 cio ´ n General para la Biodiversidad, Madrid Vila ` M, Burriel JA, Pino J, Chamizo J, Llach E, Porterias M, Serrano-Montes JL, Olmedo-Cobo JA, Go ´ mez-Zotano J (2016) Vives M (2003) Association between Opuntia species ´ ´ El analisis de la distribucion espacio-temporal y de la invasion and changes in land-cover in the Mediterranean ´ ´ percepcion social de las especies invasoras a traves de los region. Glob Change Biol 9:1234–1239 medios de comunicacion: el caso de Opuntia ﬁcus-indica y Volchansky CR, Hoffmann JH, Zimmermann HG (1999) Host Dactylopius opuntiae en Espan ˜ a. Avances en biogeografıa. plant afﬁnities of two biotypes of Dactylopius opuntiae Areas de distribucion: entre puentes y barreras. Universi- (Homoptera: Dactylopiidae): enhanced prospects for bio- dad de Granada logical control of Opuntia stricta (Cactaceae) in South Shaw RH, Bryner S, Tanner R (2009) The life history and host Africa. J Appl Ecol 36:85–91 range of the Japanese knotweed psyllid, Aphalara itadori Wheeler AG, Whitehead DR (1985) Larinus planus (F) in North Shinji: potentially the ﬁrst classical biological weed control America (Coleoptera: Curculionidae) and comments on agent for the European Union. Biol Control 49:105–113 biological control of Canada thistle. Proc Entomol Soc Shaw RH, Tanner R, Djeddour D, Cortat G (2011) Classical Wash 87(4):751–758 biological control of Fallopia japonica in the United Williams F, Eschen R, Harris A, Djeddour DH, Pratt C, Shaw Kingdom—lessons for Europe. Weed Res 51:552–558 RH, Varia S, Lamontagne-Godwin J, Thomas S, Murphy S Shaw R, Schaffner U, Marchante E (2016) The regulation of (2011) The economic cost of invasive non-native species to biological control of weeds in Europe—an evolving land- England, Scotland and Wales. CABI published report. scape. Bull OEPP/EPPO 46:254–258 (http://www.nonnativespecies.org/downloadDocument. Sheppard AW, Shaw RH, Sforza R (2006) Top 20 environ- cfm?id=487) mental weeds for classical biological control in Europe: a Zamar MI, Hernandez MC, Sotorodriguez GA, Retana-Salazar review of opportunities, regulations and other barriers to AP (2013) A new neotropical species of Liothrips (Thy- adoption. Weed Res 46:93–117 sanoptera: Phlaeothripidae) associated with Ludwigia Sohn JC, An SL, Li JE, Park KT (2002) Notes on exotic species, (Myrtales: Onagraceae). Rev Soc Entomol Argent Ophraella communa LeSage (Coleoptera: Chrysomelidae) 72:83–89 in Korea. Korean J Appl Entomol 41:145–150 Zhou ZS, Guo JY, Chen HS, Wan FH (2010) Effects of tem- Spodek M, Ben-Dov Y, Protasov A, Mendel Z (2014) First perature on survival, development, longevity and fecundity record of Dactylopius opuntiae (Cockerell) (Hemiptera: of Ophraella communa (Coleoptera: Chrysomelidae) a Coccoidea: Dactylopiidae) from Israel. Phytoparasitica potential biological control agent against Invasive rag- 42:377–379 weed, Ambrosia artemisiifolia L. (Asterales: Asteraceae). Story JM (1984) Collection and redistribution of Urophora Environ Entomol 39:1021–1027 afﬁnis and U. quadrifasciata for biological control of Zhou ZS, Guo JY, Zheng XW, Luo M, Chen HS, Wan FH spotted knapweed. Montana Sta. Univ. Coop. Ext. Ser., (2011) Re-evaluation of biosecurity of Ophraella com- Circ. 308 muna against sunﬂower (Helianthus annuus). Biocontrol Suckling M, Sforza RFH (2014) What magnitude are non-target Sci Technol 21(10):1147–1160 impacts from weed biocontrol? PLoS ONE 9(1):e84847 Zhou ZS, Chen HS, Zheng XW, Guo JY, Guo W, Li M, Wan FH Tanner RA, Varia S, Eschen R, Wood S, Murphy ST, Gange AC (2014) Control of the invasive weed Ambrosia artemisi- (2013) Impacts of an invasive non-native annual weed, ifolia with Ophraella communa and Epiblema strenuana. Impatiens glandulifera, on above- and below-ground Biocontrol Sci Technol 24(8):950–964 invertebrate communities in the United Kingdom. PLoS Zimmermann HG (1981) The ecology and control of Opuntia ONE 8(6):e67271 aurantiaca in South Africa in relation to the cochineal Tanner RA, Ellison CA, Seier MK, Kova ´cs GM, Kassai-Ja ´ger E, insect Dactylopius austrinus. PhD Thesis, Rhodes Berecky Z, Varia S, Djeddour D, Singh MC, Csisza ´rA, University, Grahamstown, 154 pp. Csontos P, Kiss L, Evans HC (2014) Puccinia komarovii Zimmermann HG, Moran VC (1991) Biological control of var. glanduliferae var. nov.: a fungal agent for the prickly pear, Opuntia ﬁcus-indica (Cactaceae), in South Africa. Agric Ecosyst Environ 37:29–35 123 Weed biological control in the European Union: from serendipity to strategy 347 Corin F. Pratt is an invasive species research scientist, Zimmermann HG, Moran VC, Hoffmann JH (2001) The renowned cactus moth, Cactoblastis cactorum (Lepi- specialising in weed biocontrol and manages the Azolla doptera: Pyralidae): its natural history and threat to native Control service at CABI. Opuntia ﬂoras in Mexico and the United States of America. Fla Entomol 84:543–551 Urs Schaffner is head of the Ecosystem Management section at CABI in Switzerland and has some 25 years of experience in weed biocontrol. Richard H. Shaw is an applied entomologist working on weed biocontrol with CABI for 23 years and is currently Country Rene´ F. H. Sforza is a research entomologist with USDA- Director UK and Regional Coordinator for invasive species. ARS, working both on weed and insect pest biocontrol. Carol A. Ellison has worked at CABI as a plant pathologist for Vicente Deltoro works for the Wildlife Service of the 30 years, using fungi to manage invasive alien weeds. Generalitat Valenciana focussing on invasive species manage- ment and habitat restoration in the region. Helia Marchante has been a researcher on invasive plants for 20 years, with a special focus on biocontrol of wattles.
– Springer Journals
Published: Oct 20, 2017