Japanese knotweed biocontrol Progress to date Lindsey Norgrove, Dick Shaw, René Eschen, Ghislaine Cortat, Alex Brook

CBC activity in Europe Insect BCA history Weed BCA history Country Recipient Source Austria 48 Finland 5 France 111 Germany 46 Greece 29 Italy 71 Portugal 18 Spain 9 Sweden 3 UK 1 41 Total 381 In Europe for Insects there have been more than 300 releases of more than 150 predators and parasitoids with very little regulation European settlers not only have a long history of starting invasions around the world but also of doing something about them as shown by this very unbalanced table of weed biocontrol releases

Weed CBC - Long and extensive history Over the past 100 years, more than 400 different biocontrol agents have been used against around 150 target plants, totalling over 1,300 introductions around the globe. Weed biocontrol is not a novel approach and over the past century there has been a lot of activity

This is a typical shot of the unruly knotweed ignoring the rules of the road and as one of the worst weeds in the world it was an excellent candidate for the first target for this approach in the EU. It costs GB a little over £165 million (188 million euro) and is famed for damaging the built environment

It costs GB a little over £165 million (188 million euro) and is famed for damaging the built environment

Cost of Japanese knotweed to GB 92% of the £166 million annual costs are experienced by the construction and development industry.

A consortium of Sponsors came together in 2003 to sponsor the programme After many years of project development activity a consortium of sponsors came together to fund the biocontrol programme and CABI won the tender. British Columbia are also sponsors but don’t have a logo

As is always the case, It soon became clear that Japanese knotweed had many more natural enemies in its native range than here and our job was to find the safest and most effective member of that group

Many insects feeding on most parts 186 species of phytophagous arthropod recorded from Japanese knotweed in Japan. Of the many species of arthopods which are found damaging the plant in Japan there were almost no root feeders surprisingly but most other parts of the plant were attacked to some degree.

Collaboration was essential

A process of elimination Biocontrol comes down to a process of elimination whereby most potential agents are dismissed in the early stages and don’t ever make it to the laboratory study stage. Because of time constraints this presentation will not cover the years of research that led to us dismissing potential agents even at the late stage.

In the interests of safety, the testing work was carried out in our Defra-licensed level 3 quarantine facilities alongside field work carried out by our collaborators in Japan

I won’t deal with fungi in the short time I have today but as you can see from our lead pathogist’s face there were some exciting species found and the inset mycosphaerella leafspot remains a very damaging and promising potential agent it was just a little harder to work on but it should be noted that fungi have an excellent track record in weed biocontrol

Aphalara itadori All of that painstaking research narrowed our options down to the sap-sucking psyllid A. itadori which is named after its host – always a good sign

The adult is really just an egg-laying machine and it is her offspring, the nymphs that do the damage as they pass through their 5 developmental stages, sucking the sap and generating the white wax you can see in this slide

Test Plant List 90 species and varieties representatives from 19 families. 37 plants natives including all native Polygonaceae 23 species introduced to the UK, 3 species native to Europe, 13 ornamental 10 economically important UK species No means of agreeing the test plant list in advance! Drawing up the test plant list based on phylogeny resulted in 89 species being tested including some American test plant species. This is a very long test plant list and includes some species that have some cultural value despite being quite distantly related

Aphalara adult survival

The 78 spp. that did not receive eggs are excluded This graph summarises 4 years of work following over 145,000 eggs. This shows the results of the multiple choice oviposition studies and only includes those species which ever received any eggs. Note the rapid drop off from the 430 or so eggs laid on the target plant. To the right of the red line no adults were produced and to the left only invasive knotweeds, varieties or hybrids could support complete development from egg to adult. Therefore we can conclude that the psylid is incapable of maintaining a population on anything other than the target weed(s) Bar chart showing mean egg count on those plants that did receive eggs in multiple choice oviposition tests. (+/- 1SE). Development only successful to the left of red line

Nymph %survival over time

R2= 0.9328 Dev Rate per day = 0.01921+0.002162 Temp DD 462.5 from egg to adult

Licensing: The two processes (England) Licence to release into the wild under the Wildlife and Countryside Act 1981 Licence to free it from a Plant Health Quarantine license as “an organism likely to be injurious to plants in the UK” - EU Standing Committee on Plant Health were kept informed No for the complex but effective licensing process which became more straightforward once it was dettermined that Plant health Legislation was appropriate. These two pathways had to be cleared simultaneously baciase without one licence granted the other would not permit release into the wild See also: Hunt et al (2010) An international comparison of invertebrate biological control agent regulation: what can Europe learn? REBECA.

W&C Act application for release Based on Eppo template Pest Risk Analysis W&C Act application for release Based on Eppo template Brand new version for Wales & England Internal Govt iterative review ACRE Committee review External Peer review Public consultation (3 months) Chief Scientist advice Ministerial decision for Sec. of State Release from PH quarantine licence W&C license to release The EPPO – based PRA was the best tool for the job as it is widely recognised despite not being designed for a “beneficial pest”. As can be seen there was intense consultation including a full public consultation alongside peer reviews and it was useful that a peer-reviewed paper supported the application

2o & 3o and community level effects? Choice tests with commercially available generalists showed no feeding preference Native coccinellids fed exclusively on psyllids fared worse than when fed on aphids

One requirement of the license was that a 5 year monitoring plan was agreed and fully funded. The plan agreed represents one of the most thorough post- release monitoring plan in weed biocontrol history and is designed to detect any negative impact as well as record the efficacy of the agent over time. There was also a requirement for a contingency plan which requires the treatment of any affected sites with insecticide and a follow-up herbicide treatment should any significant adverse effects be observed (this is the first time such a contingency has been used to our knowledge). A combination of fixed quadrats and repeat sampling with vortice and reverse leaf-blowers is being used to record all arthropods whilst vegetation surveys cover the flora. In Phase 1 Fallopia dumetorum (red data book sp.) and F. convolvulus plants + and – insecticide were planted out at release and any impact recorded.

Caged no-choice & Choice experiment Oviposition and development of A. itadori and non-target impact on F. dumetorum As a result of the late frost in may which removed the knotweed leaves at release sites and therefore most of the eggs, we decided to carry out caged studies alongside applying for additional release at one site in higher numbers. This would ensure useful data was generated outside the comfort of the lab. This involved the use of the most important native Fallopia sp. And requent measuring, production of cages and sleeves very labour-intensive. Ca. three-four people for three days every fortnight for three months.

Caged no-choice experiment Many eggs, some nymphs, limited development F. dumetorum In the extreme example of no-choice tests plenty of eggs were laid on the non-target in the absence of its normal host but as expected very few nymphs developed and none made it to adult. Grey bars eggs, black bars nymphs

Comparison with pre-release quarantine multiple-choice tests Patterns in oviposition similar No complete development on any non-target species Very similar to published studies 1.9% 0.2% 1.6% 0.4% 0 (2)% 0 (1)% Quarantine Caged Open field Redrawn from Shaw (2009) Eggs two (four) weeks after start In the more realsitic multiple choice study with both non-target Fallopia spp. we found almost identical results as we generated in quarantine. This is one of the first times such a comparison has been made that was not retrospective.

Host-specificity testing Quarantine Caged Open field No-choice Multiple choice Fundamental host range Realised host range Our experiments span the whole range of specificity tests done in other weed biological control programmes and all show that the risk to native ecosystems is very low Artificial Natural Host-range tests reliably predict non-target attack (Pemberton 2000; Fowler et al. 2000; Barton 2004; Briese 2005) Non-target attack either “predicted” or ephemeral

Summary Caged and open-field studies confirm the host-specificity of Aphalara itadori No impact of the psyllid on non-target plant species No impact of A. itadori on native vegetation or invertebrate community Risk of non-target impact on native vegetation and invertebrates very low In summary

No A. itadori found in winter sampling Typical sample from evergreens contained 100s native psyllids, but no A. itadori Species sampled included: yew, Pinus spp., Leyland cypress, etc. Disappointing but it is like finding a needle in a haystack at this stage Low abundance of A. itadori at release sites  larger releases required for establishment

Successful overwintering!! The latest news is that in early April during our first visit to the field we saw adult Aphalara at the site which had received the most adult psyllids (6,000) which means that they had successfully overwintered

Mass-producing psyllids Two production cycles: First in cages inside Controlled environment We are currently reaching the end of the mass production facility and have begun our Phase 2 widespread releases thanks to the mass-rearing that has been going on over the past 3 months.

Mass-producing psyllids Data loggers allow checks on development Insects to be ready for releases in last two weeks in May

What can we expect? If successful: Establishment of the agent Spread to JK Reduced plant vigour Reduced control costs Recovery of native species Control not eradication! Biocontrol is a long term solution to very large scale problems and as such is not a quick fix. But if released we would hope to see damaged and less invasive knotweed within a few years. Even if its rate of spread is reduced then it would have been worthwhile. A 1% reduction in costs in GB will have paid for the project in less than a year.

EU opportunities Sheppard, Shaw & Sforza - Weed Research 2006 Species Form Origin EU distribution Genus native? Conflict BC history Buddleja davidii Ph China Temperate Nob O Yes Fallopia japonica Ge Japan No Acacia dealbata Australia Mediterranean Yesd Azolla filiculoides Hy N America Temp/Med Ailanthus altissima Impatiens glandulifera He India Rhododendron ponticum S Europe Robinia pseudoacacia F Senecio inaequidens S Africa Ambrosia artemisiifolia Th C America Carpobrotus edulis Ch Heracleum mantegazzianum W Asia Solanum elaeagnifolium S America Tem/Med Baccharis halimifolia Hydrocotyle ranunculoides Ludwigia peploides Crassula helmsii Australasia Elodea canadensis Myriophyllum aquaticum Solidago canadensis There are many other targets for this approach in Europe and we can provide pdf copies of this paper if requested.

Hydrocotyle ranunculoides In GB we are actively researching other targets such as Floating Pennywort Photo – T. Renals

For which a South American weevil looks to be very promising

Impatiens glandulifera Himalayan balsam is another excellent target and extensive research in the Himalayas has revealed a rust fungus

Puccinia rust Which is currently undergoing late stage testing in our quarantine facility

Thank you to all involved Dr Harry Evans (CABI), Dr Marion Seier & Dr Rob Reeder Rob Tanner (CABI) Djamila Djeddour (CABI) Dr Carol Ellison Drs Murphy, Cock and Holderness (CABI) Ghislaine Cortat (CABI) Dr Rene Eschen Anna Harris Sonal Varia Corin Pratt Alex Brook Dr Esther Gerber Valérie Coudrain & Sarah Bryner (CABI tudents) Sasha White Dr Paul Cannon and Dr Alan Buddie (CABI) Linda Birken (Imperial College student) Gareth Martin (Imperial College student) James Broom (Imperial College student) Dr John Bailey and Kat Pashley (Leicester University) Dr Lois Child (Loughborough University) Dr Andy Polaszek & others (NHM) Professor Masami Takagi (Kyushu University) Dr Daisuke Kurose (Kyushu University) Dr Narutu Furuya (Kyushu University) Dr Naoki Takahashi (Kyushu University) Yuko Inoue (Kyushu University) Dr Fritzi Grevstad (University of Washington) Dr Bernd Blossey (Cornell University) Dr Rob Bouchier (AAFC Canada) Dr Brian Van Hezelwink (AAFC Canada) Victoria Nuzzo (Independent Consultant) Mic Julien (CSIRO) Dr Andy Sheppard (CSIRO) Dr Simon Fowler (Landcare Research NZ) Drs Ted Centre & Gary Buckingham (Florida Uni) Profs Mick Crawley &Tim Coulson (Imperial College) Dr Willie Cabrera Walsh (SABCL) Dr Jonathan Newman (CEH) Dr Usha Dev (NBPGR) Dr Ravi Kheterpal (NBPGR) Dr Robin Adair (DPI Queensland) Drs John Ireson & Richard Holloway (Utas) Lindsay Smith (Landcare Research) ACRE FERA – many especially Dr Claire Sansford Pesticide Safety Directorate The Non Native Species Secretariat The Project Board and sponsors for funding and guidance As with any long term international research there are a lot of people to thanks.

Thank You Any Questions? A multilingual Thank You slide is available in the CABI Resources site (www.cabi.org/commercial)