Biocontrol of escaped ornamentals Plants that have escaped from gardens and are invading wild habitats are inevitable subjects for biological control. Richard Shaw and Robert Tanner have these difficult targets in their sites

s global trade increases, refer to a more modest 1,377 Increasing pressure the movement of species and established non-native plants. There is no getting away from the A their introduction to new Most invasive plants have been fact that our passion for horticultural regions is on the rise. Countries introduced for horticultural use by novelties has resulted in an increase with longer trading histories and nurseries, botanical gardens, and in propagule pressure of potential historically better wealth tend to be individuals (Reichard & White invasive weeds. However, we should the ones with the most alien species. 2001) and this pathway is well recognize that, on average, only 10% The UK is a shining example in recognized in the UK (Dehnen- of new arrivals are able to hop the Europe with more alien plant and Schmutz et al. 2007). As a result, a garden fence and only 10% of these species (3,524) than any other voluntary code of conduct has been can establish and become invasive. European nation, a clear 600 more proposed for Europe (PM 3/74(1), Despite this low percentage, the than the closest rivals France and 2009). The RHS recognized the worry is that we have been receiving Belgium (DAISIE, www.europe- problem early and banned a list of exotic species from far-flung corners aliens.org). Unsurprisingly, plant taxa least-wanted weeds from sale at its of the world for centuries, and many are the largest component of these outlets, long before an actual ban on species do not show their true lists worldwide. The UK has 1,834 sale became a reality in England in invasive potential until many (DAISIE) although Roy et al. (2102) February 2013. decades after introduction. The

220 December 2013 PlantsmanThe

Japanese knotweed (left) is already being of origin of the target weed. This representatives of other orders. If targetted in the UK by a recently released psyllid biogeographical challenge involves significant feeding and development , Aphalara itadori (nymphs and adult, insets) using molecular tools, as well as good is recorded on any test plant then spread of invasive weeds tends to be old-fashioned detective work in the the species will be dropped. As a exponential. This means that the great herbaria of the world. result of this ‘centrifugal phylogen­ early stages of invasion are impercep­ Permissions then need to be secured etic host-range testing process’ it is tible until one doubling event leads and any access and benefit sharing common for more than 100 natural to a perceived explosion. There are issues, under the Nagoya Protocol of enemies to be thinned down to one exceptions, such as Hydrocotyle the Convention on Biological or two potential candidates. That is ranunculoides which only arrived in Diversity, cleared up. not to say all will be tested, as many the 1980s and was soon recognized Entomologists and plant pathol­ natural enemies will be identified as as a serious threat to our waterways. ogists then carry out extensive polyphagous species from the natural-enemy surveys in the native literature and therefore they will not Classical biological control range throughout the growing season warrant further consideration, or Once a plant species has arrived, of the plant. Collaborators in the they will be impossible to culture, or established, and spread beyond the host country support the research, have no impact on the target weed. bounds of feasible eradication, it is often conducting additional surveys tempting to say that it is beyond to ensure potential agents are not Japanese knotweed control reasonable control. It can often missed. As it is often the case that It is perhaps appropriate to use become the elephant in the room little is known about many of these Japanese knotweed (Fallopia japonica while decision-makers focus on what species, they are carried by person var. japonica) as a means of demon­ they think they can deal with, such under a Plant Health licence to a strating the process. A search for a as prevention and early detection or secure quarantine unit. Here they biocontrol agent was recently carried eradication. This leaves land are reared for identification and out for the UK and culminated in All photographs by CABI staff managers with a growing problem, assessed for safety. This testing stage the release of the specialist psyllid and only chemical or mechanical is the most laborious and expensive insect, Aphalara itadori. tools to deal with whatever their of all the work carried out. Following promising surveys in budget and patience will allow. Japan, the plant’s native range, in Fortunately, all may not be lost. Testing phase 2000, a consortium of stakeholders In some cases nature may have Of course, it is impossible to came together in 2003 to fund a already provided the solution. This evaluate all plant species in the UK biocontrol project. The stakeholders’ is usually in the form of natural as unintended targets. Therefore, aim was to control the plant in enemies that were left at home molecular and morphological England, Wales, USA and Canada. when the species was cleaned up and is used to draw up a plant 186 species of and more propagated for its new range. The list against which potential agents than 40 species of fungi were use of these exotic natural enemies are tested. are tested for recorded in Japan (Shaw et al. 2009). in weed management is known as feeding, egg-laying and subsequent A list of 90 plant species to test was classical biological control (CBC). development, and fungi are tested compiled, which included all native This method has been implemented for infection and sporulation. The members of the Polygonaceae, the against nuisance weed species most important group of plants to knotweed family. This list is longer worldwide for more than a century. test is those most closely related to than similar lists compiled by other However, until recently there had the target weed, especially if they projects because it was the first time been no use of this tried and tested have a similar life cycle or are morph­ a CBC programme had been technology in any EU member state. ­ologically similar to the target species. implemented in Europe against a After this, testing moves out to weed. The inclusion of crops and Primary research include members of the same iconic species was deemed The first job of biocontrol subtribe, tribe, subfamily, family appropriate to reassure the public, practitioners is to identify the area and eventually includes even though they could be considered scientifically irrelevant Floating pennywort, Hydrocotyle ranunculoides, due to their phylogenetic separation exhibits extraordinary growth rates from the target weed. Adult ➤

December 2013 221 Water fern, Azolla filiculoides, can die back suddenly when a weevil, Stenopelmus rufinasus (inset), takes hold. The left-hand picture was taken on 26 July, the right-hand one on 22 August survival, multiple choice oviposition Small-scale releases took place with target present and absent, in 2010 at two sites, and on a larger starvation tests, and larval transfer scale at eight sites in 2011 and in and development studies were 2012. A much larger population carried out. More than 70,000 was released at the eight sites in an eggs were observed and counted. attempt to push the population over We concluded that the psyllid was a threshold where it would become a true specialist on Fallopia japonica, established. The sites have not been F. x bohemica and, to a lesser extent, made public, to protect them and under the current license until it F. sachalinensis. the data being generated. These are becomes ordinarily resident. It can A pest risk analysis was produced very early days as biocontrol agents then be moved around, without in order to free the psyllid from can take 5–10 years to establish and restriction, to sites that it is not quarantine licence. Also, an applicat­ spread. However, adults have been naturally colonizing. ion for field release was made under shown to overwinter successfully, Hopes are still high for success, the Wildlife and Countryside Act. which is a crucial first step. and the US and Canada have The dossiers were scrutinized by the Once the psyllid enters its maintained interest and their Food and Environment Research expansive phase, local recorders authorities are being petitioned for Agency (Defra) and various consult­ and the general public will be asked release. In the meantime, research ing public bodies. They were then to engage in the monitoring continues, in quarantine, on a sent to the Advisory Committee on programme, reporting any sightings common leafspot from Japan which Releases to the Environment who to a central recording office. It is could prove to be an important requested a little more research on important to note that the psyllid is complement to the psyllid – results the potential effects mediated not for sale, and its redistribution is so far are encouraging. through generalist native predators. Once they were satisfied there was a further peer review by anonymous independent biocontrol experts, most probably including some from overseas, and the whole proposal went to public consultation for three months. After this, the government Chief Scientist gave his opinion and the release was authorized in England, and shortly afterwards in Wales, in 2009. The release license required a 5-year fully-funded monitoring and contingency plan to Australian swamp stonecrop, Crassula helmsii, might succumb to a stem-boring fly,Hydrellia perplexa (inset) be implemented, which is on-going.

222 December 2013 A Puccinia rust fungus (inset) is showing promise as a potential biocontrol for Himalayan balsam, Impatiens glandulifera

goal is never eradication but the a stem-boring fly and eriophyid mite Himalayan balsam suppression of the plant to the point are looking promising, along with a Defra is currently funding three where it behaves more like it does in suite of fungal pathogens. biocontrol projects against weeds. its native range. These may influence achieving the Floating pennywort Water Framework Directive target Australian swamp stonecrop Hydrocotyle ranunculoides is a relative of reaching good ecological status on Crassula helmsii is a submerged and newcomer but is one of the most our inland and marine waterways. emergent aquatic weed that seems to vigorous invaders. Its remarkable Himalayan balsam (Impatiens specialize in habitats with high growth rate enables it to choke glandulifera) is perhaps the most conservation status. It is the bane of kilometres of canal and drainage advanced of these. Surveys in the many reserve managers. It is also ditches in a single season. Indian and Pakistani Himalayan known as New Zealand pigmyweed A weevil, Listronotus elongatus, is foothills have revealed a Puccinia rust but molecular biogeography suggests the lead candidate in this case, not fungus which is autoecious, meaning that the version naturalized in the least because weevils and floating it completes all of its life stages on UK is of Australian origin. aquatic weeds appear to be a perfect the same host. Spores overwinter in Pigmyweed did not look like a match. Weevils have successfully the litter to infect and distort young good target due to an old scientific controlled some of the worst seedlings in the spring. Following paper stating there were no natural invaders around the world such as this infection phase, spores go on to enemies in its native range. However, Eichhornia crassipes, Pistia stratiotes infect the leaves, debilitating the the first site that was surveyed in and Salvinia molesta. Nevertheless, plants, ultimately reducing their Victoria revealed a stem-boring a suite of stem-boring flies and a rare competitive potential and likely seed weevil that may be new to science. rust fungus are also in the frame, but production. As ever, the ultimate This is a common occurrence in gaining permission to export these biocontrol surveys as these plants are agents from South America has often not well-studied. delayed progress until recently. Unfortunately, the weevil has been Work carried out in 2006 suggested dismissed after screening revealed that our native Hydrocotyle vulgaris is that it also feeds on Sedum. However, not a suitable host for the weevil, so this remains one of the most exciting current projects.

Giant hogweed Heracleum mantegazzianum is a serious problem for human health. Weevils have shown good form in controlling This is due to its phytophototoxic aquatic weeds, so Listronotus elongatus sap which can cause serious might thrive on floating pennywort, blistering if it contacts body parts Hydrocotyle ranunculoides (left) that are then exposed to sunlight. ➤

December 2013 223 The search for a biocontrol of giant Himalayan knotweed, Persicaria hogweed, Heracleum mantegazzianum, polystachya, is behaving worryingly is ongoing like Japanese knotweed in Cornwall

Affected parts can be permanently The complete removal of a to run an ageing railway or preserve discoloured. biocontrol agent’s host plant is not historic buildings. In both cases, Unfortunately, it seems that no normal. It leads to the agent’s demise the use of exotic natural enemies suitable agents exist in its native as it is unable to feed on any other for their permanent control would range of the Caucasus. Our work host plant. This is why this agent has probably not be acceptable unless on the most promising candidate, to be redistributed. Nonetheless, a voracious specialist seed-feeder a Phloeospora fungus, revealed it was this atypical example does could be found. unable to attack the closely related demonstrate the safety and potential Research has therefore focused Heracleum sphondylium but could of biocontrol to a doubting public. on trying to develop fungal stump infect parsnip, Pastinaca sativa. treatments to rot the cut material Interestingly, this suggests Pastinaca Rhododendron and Buddleja away after cutting, thereby is much closer to Heracleum than One of the other challenges facing preventing resprouting. This is in traditional phylogeny would suggest. biocontrollers is what we call stark contrast to New Zealand conflict-of-interest weeds, i.e. those where a leaf-feeding weevil has been Water fern that are both troublesome and released against Buddleja davidii and The azolla weevil, Stenopelmus valued. Perhaps the best example is is having a devastating impact on rufinasus, provides an unusual Rhododendron x superponticum (a recent even the largest bushes. example of biocontrol. It has been name for the invasive plant, which is on our shores since at least 1921, actually a hybrid of R. ponticum). Other ornamental targets eating water fern, Azolla filiculoides, Having escaped from gardens it now Sheppard et al. (2006) proposed the largely unnoticed. It was clearly not invades woodland and hillsides, top 20 weed biocontrol targets for doing a good enough job as water threatening habitats such as Atlantic Europe. Some should be of interest fern is still a problem in still or slow- oak woodland and harbouring the to the UK. Tree of heaven, Ailanthus moving waterbodies in the UK. devastating Phytophthora ramorum altissima, is already establishing in the However, there are many and P. kernoviae pathogens. wild in the UK. It is a problem in anecdotal reports of water fern being Nonetheless, coach-loads of warmer climes so is one to watch a problem on ponds, turning brown domestic tourists travel to under likely climate change or red as usual, and then vanishing. Snowdonia just to see it bloom. scenarios. It is a serious weed in the These cases are almost certainly due Buddleja davidii is another US where research has shown that a to the weevil. It is now redistributed example, where its value to gardeners weevil, Eucryptorrhynchus brandti, is for Azolla control on even the most is revealed in its common name of highly specific. sensitive sites with great success (see butterfly bush. But it is the last Three targets in waiting are www.azollacontrol.com). invader you want if you are trying hottentot fig, Carpobrotus edulis,

224 December 2013 PlantsmanThe which smothers rocky cliffs; mentioning the cane toad, environmental and economically goldenrod, Solidago, which is a introduced to Australia to control impact of invasive plants, far problem in eastern Europe; and sugar-cane . The use of any outweighed the small risk of Himalayan knotweed, Persicaria vertebrate predator is misguided non-target impact. wallichii (syn. Polygonum polystachyum), because it is not going to stick to the which has developed some serious one species you want to control. Its Conclusion infestations in Cornwall. All have introduction was carried out without In summary, numerous plant species known natural enemies in their native any of the risk assessments required have been introduced because of range. With climate change they today, and was against some scientific their beauty or impressive stature, may spread to become bad enough opinion at the time. Next to modern not forgetting that Japanese to be considered for biocontrol. weed biocontrol it is like comparing knotweed won the best newcomer the risks of wind and nuclear power. award at the Utrecht flower festival Bad news stories A better example of biocontrol in the late 1800s. Some have shown It is rare for a journalist to cover the going wrong is the use of harlequin their invasive potential after a long subject of weed biocontrol without ladybird. Originally used inside lag phase, but we are likely to have glasshouses, its use outside has had built up a significant invasion debt references devastating consequences on native with sleeper weeds waiting to enter Clewley, GD, Eschen, R, Shaw, ladybirds across Europe. It even their expansion phase. Gardeners RH & Wright, DJ (2012) The taints wine in California when should recognize the risk and ensure effectiveness of classical biological squashed alongside the grapes. The that when plants need to be disposed control of invasive plants. J. Appl. Ecol. 49: 1287–1295 use of against insects has a of they are composted or destroyed Dehnen-Schmutz, K, Touza, J, long history in Europe and more in the garden. Perrings, C & Williamson, M than 350 introductions have been Biological control, when practiced (2007) The horticultural trade and made into the environment against properly, offers a safe, environment­ ornamental plant invasions in Britain. more than 50 pest species (Gerber & ally sound and economically Conserv. Biol. 21: 224–231 Schaffner, pers. comm.), most sustainable potential solution to a PM 3/74(1) (2009) EPPO guidelines without any host-range testing. growing problem (see Clewley et al. on the development of a code of In the case of weed biocontrol, 2012). The knotweed psyllid release conduct on horticulture and invasive alien plants. OEPP/EPPO Bulletin there have been more than 1,400 has shown that such an approach is 39: 263–266 releases against more than 350 weed possible in Europe and should open Reichard, SH & White, P (2001) targets. There are only a dozen the door to the wider use of this Horticulture as a pathway of invasive reported cases of non-target attack tried and tested, century-old plant introductions in the United and almost all of them were technology. States. Bioscience 51: 103–113 predicted by researchers. However, Gardeners should be reassured Roy, HE et al. (2012) Non-native the need for control, to reduce the that the pest risk analyses applied to species in Great Britain: establishment, detection and reporting to inform biocontrol agents is very thorough. effective decision making. Report to acknowledgements The risk to their garden plants is Defra. Centre for Ecology and Most of the work reported above was vanishingly small, unlike the risk Hydrology, Wallingford funded by Defra. The original Fallopia posed to our delicate environment Shaw, RH, Bryner, S & Tanner, R project was funded by a consortium by a small minority of those plants (2009) The life history and host range including Defra, Environment we initially value, but which of the Japanese knotweed psyllid, Agency, Welsh Assembly ultimately leap the fence. Aphalara itadori Shinji: potentially Government, Network Rail, Canal & the first classical biological weed Rivers Trust, South West Regional control agent for the European Development Agency, and Union. Biol. Control 49: 105–113 coordinated by Cornwall Council. Dr Richard Shaw is Regional Sheppard, AW, Shaw, RH & Additional funders include the Coordinator for Invasive Species and Sforza, R (2006) Top 20 environ­ USDA Forest Service in the US and Deputy Director at CABI E-UK mental weeds for classical biological the Ministry of Forests, Land and Dr Robert Tanner is Senior control in Europe: a review of opport­ Natural Resource Operations, in Scientist and Project Manager for unities, regulations and other barriers British Columbia, Canada, as well the Himalayan balsam biological to adoption. Weed Res. 46: 1–25 as the Scottish Executive. control project at CABI E-UK

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