APPLICATION FORM Release

To obtain approval to release new organisms (Through importing for release or releasing from containment)

Send to Environmental Protection Authority preferably by email ([email protected]) or alternatively by post (Private Bag 63002, Wellington 6140) Payment must accompany final application; see our fees and charges schedule for details.

Figure 1. Buds and leaves of old man’s beard deformed by Aceria vitalbae galls. Source: Mihajlovic et al. 1998

Application Number

APP203313

Date

20 June 2018

www.epa.govt.nz 2

Application Form Approval to release a new organism Completing this application form

1. This form has been approved under section 34 of the Hazardous Substances and New Organisms (HSNO) Act 1996. It covers the release without controls of any new organism (including genetically modified organisms (GMOs)) that is to be imported for release or released from containment. It also covers the release with or without controls of low risk new organisms (qualifying organisms) in human and veterinary medicines. If you wish to make an application for another type of approval or for another use (such as an emergency, special emergency, conditional release or containment), a different form will have to be used. All forms are available on our website. 2. It is recommended that you contact an Advisor at the Environmental Protection Authority (EPA) as early in the application process as possible. An Advisor can assist you with any questions you have during the preparation of your application including providing advice on any consultation requirements. 3. Unless otherwise indicated, all sections of this form must be completed for the application to be formally received and assessed. If a section is not relevant to your application, please provide a comprehensive explanation why this does not apply. If you choose not to provide the specific information, you will need to apply for a waiver under section 59(3)(a)(ii) of the HSNO Act. This can be done by completing the section on the last page of this form. 4. Any extra material that does not fit in the application form must be clearly labelled, cross-referenced, and included with the application form when it is submitted. 5. Please add extra rows/tables where needed. 6. You must sign the final form (the EPA will accept electronically signed forms) and pay the application fee (including GST) unless you are already an approved EPA customer. To be recognised by the EPA as an “approved customer”, you must have submitted more than one application per month over the preceding six months, and have no history of delay in making payments, at the time of presenting an application. 7. Information about application fees is available on the EPA website. 8. All application communications from the EPA will be provided electronically, unless you specifically request otherwise. Commercially sensitive information

9. Commercially sensitive information must be included in an appendix to this form and be identified as confidential. If you consider any information to be commercially sensitive, please show this in the relevant section of this form and cross reference to where that information is located in the confidential appendix. 10. Any information you supply to the EPA prior to formal lodgement of your application will not be publicly released. Following formal lodgement of your application any information in the body of this application form and any non-confidential appendices will become publicly available.

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Application Form Approval to release a new organism

11. Once you have formally lodged your application with the EPA, any information you have supplied to the EPA about your application is subject to the Official Information Act 1982 (OIA). If a request is made for the release of information that you consider to be confidential, your view will be considered in a manner consistent with the OIA and with section 57 of the HSNO Act. You may be required to provide further justification for your claim of confidentiality. Definitions

Restricting an organism or substance to a secure location or facility to prevent Containment escape. In respect to genetically modified organisms, this includes field testing and large-scale fermentation

Any obligation or restrictions imposed on any new organism, or any person in relation to any new organism, by the HSNO Act or any other Act or any Controls regulations, rules, codes, or other documents made in accordance with the provisions of the HSNO Act or any other Act for the purposes of controlling the adverse effects of that organism on people or the environment

Any organism in which any of the genes or other genetic material:  Have been modified by in vitro techniques, or Genetically Modified  Are inherited or otherwise derived, through any number of replications, from Organism (GMO) any genes or other genetic material which has been modified by in vitro techniques

As defined in section 3 of the Medicines Act 1981 Medicine http://www.legislation.govt.nz/act/public/1981/0118/latest/DLM53790.html?src=qs

A new organism is an organism that is any of the following:  An organism belonging to a species that was not present in New Zealand immediately before 29 July 1998;  An organism belonging to a species, subspecies, infrasubspecies, variety, strain, or prescribed as a risk species, where that organism was not present in New Zealand at the time of promulgation of the relevant regulation;  An organism for which a containment approval has been given under the HSNO Act;  An organism for which a conditional release approval has been given under the HSNO Act; New Organism  A qualifying organism approved for release with controls under the HSNO Act;  A genetically modified organism;  An organism belonging to a species, subspecies, infrasubspecies, variety, strain, or cultivar that has been eradicated from New Zealand;  An organism present in New Zealand before 29 July 1998 in contravention of the Act 1967 or the Plants Act 1970. This does not apply to the organism known as rabbit haemorrhagic disease virus, or rabbit calicivirus A new organism does not cease to be a new organism because:  It is subject to a conditional release approval; or  It is a qualifying organism approved for release with controls; or

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Application Form Approval to release a new organism

 It is an incidentally imported new organism

Qualifying Organism As defined in sections 2 and 38I of the HSNO Act

To allow the organism to move within New Zealand free of any restrictions other Release than those imposed in accordance with the Biosecurity Act 1993 or the Conservation Act 1987

As defined in section 2 of the Biosecurity Act 1993 Unwanted Organism http://www.legislation.govt.nz/act/public/1993/0095/latest/DLM314623.html?src=q s

As defined in section 2(1) of the Agricultural Compounds and Veterinary Medicines Act 1997 Veterinary Medicine http://www.legislation.govt.nz/act/public/1997/0087/latest/DLM414577.html?searc h=ts_act%40bill%40regulation%40deemedreg_Agricultural+Compounds+and+Ve terinary+Medicines+Act+_resel_25_a&p=1

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Application Form Approval to release a new organism 1. Applicant details

1.1. Applicant

Company Name: Horizons Regional Council

Contact Name: Craig Davey

Job Title: Natural Resources and Partnerships Coordinator

Physical Address: 181 Guyton St, Wanganui

Postal Address: Private Bag 11025, Manawatu Mail Centre, Palmerston North

Phone: 06 9524916

Fax: N/A

Email: [email protected]

1.2. New Zealand agent or consultant (if applicable)

Company Name: Richard Hill & Associates

Contact Name: Richard Hill

Job Title: Application Manager

Physical Address: 237 Ashgrove Tce, Christchurch 8024

Postal Address: 237 Ashgrove Tce, Christchurch 8024

Phone: 03 3322543 or 0211376 919

Fax: N/A

Email: [email protected]

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Application Form Approval to release a new organism

2. Information about the application

2.1. Brief application description Approximately 30 words about what you are applying to do

An application to introduce a gall mite, Aceria vitalbae, as a biological control agent for the weed old man’s beard ( vitalba).

2.2. Summary of application Provide a plain English, non-technical description of what you are applying to do and why you want to do it

This is an application by Horizons Regional Council to introduce the gall mite Aceria vitalbae as a biological control agent for the weed old man’s beard (OMB, ). This vine has woody stems that can grow 20 to 30 metres long. Vines scramble through bush margins and can readily climb over understorey plants in light gaps, even in established forests. It forms dense, permanent masses with heavily layered stems that physically smother and collapse underlying vegetation. Heavy infestations prevent regeneration, leading to loss of indigenous species from affected areas. Loss of natives opens vegetation to invasion by other weeds, modifying ecosystems. OMB can also scramble over the ground, destroying low-growing plant communities in riparian, coastal and other sensitive habitats.

Infestations of C. vitalba are common in every region of New Zealand except Northland and Auckland. C. vitalba may be the most publicised environmental weed in New Zealand, and community groups, government departments, and local authorities are trying to manage its effects. Control using a combination of mechanical and chemical methods can be effective, but it is expensive, can be damaging to associated vegetation, and cannot be applied everywhere that OMB is a threat. If successful, biological control would offer a safe and sustainable alternative. Control agents can also disperse to isolated infestations that are currently not accessible, or unknown, to weed managers.

The OMB gall mite (Aceria vitalbae) is minute, at about 1 millimetre long. Feeding by the mite induces growth abnormalities, or galls, on the buds and developing leaves of OMB (Figure 1). The mites breed within those galls. The formation of galls reduces the growth rate of the weed and may cause shoots to die back. Significant damage to OMB plants from mite attack has been observed in its native range.

Section 5 of the application explains the expected positive effects of successful biological control of OMB, including:

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Application Form Approval to release a new organism

 improved biodiversity in invaded native habitats of low stature, because of decreased competition and decreased mortality of native plants  reduced damage to native shrubs and trees caused by shading and canopy collapse resulting from OMB invasion  Improved regeneration under native vegetation, as shading by OMB is reduced  reduced OMB control costs for weed managers Introduced natural enemies become permanently established in the environment, and their effects on a target weed persist from year to year. Introduced natural enemies must therefore be safe if this weed management tactic is to be environmentally acceptable. Results of tests to confirm the range of plants susceptible to the mite, an assessment of the beneficial and adverse effects of the proposal, and the results of consultation with the community are summarised in this application. Experimental evidence indicates that the gall mite will not cause significant damage to any native plant or desirable ornamental species. The potential effects on Māori cultural values are also presented.

The application concludes that OMB gall mite will have no adverse effect on ecological, environmental, social or community values in New Zealand. OMB has no significant environmental or economic value in New Zealand. The application also concludes that the potential benefits of the introduction of OMB gall mite to New Zealand outweigh the potential risks and costs. Other information can be found on the Manaaki Whenua − Landcare Research website at http://www.landcareresearch.co.nz/science/plants- animals-fungi/plants/weeds/biocontrol/approvals/current-applications.

2.3. Background and aims of application

This section is intended to put the new organism(s) in perspective of the wider activitie(s) that they will be used in. You may use more technical language but all technical words must be included in a glossary.

2.3.1 Purpose

This application seeks approval to introduce to New Zealand a new organism, the gall-forming mite Aceria vitalbae (Canestrini), for the biological control of old man’s beard (OMB), Clematis vitalba L. The application is submitted by Horizons Regional Council on behalf of the National Biocontrol Collective. The Collective comprises 14 regional councils and the Department of Conservation (DOC). The Collective has determined that biological control is the most environmentally acceptable and sustainable means of reducing the environmental impacts of OMB in New Zealand. Manaaki Whenua − Landcare Research is the science provider for this development, and has contracted Richard Hill & Associates to prepare this application and to manage the application process on behalf of Horizons Regional Council.

OMB causes environmental damage throughout most of New Zealand, often in distant or inaccessible areas of high conservation value. Managing the effects of OMB is expensive and is not feasible on much

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Application Form Approval to release a new organism of the land infested with OMB, except to prevent the weed from establishing in un-infested areas or to protect areas of the highest biodiversity value. Most infestations of the weed are not managed at all. Biocontrol would complement existing control methods used to mitigate the negative impacts of this weed because biocontrol agents will persist once established, offering the potential to:

 suppress OMB plants in areas where control is not possible, reducing the accumulation of damaging biomass

 suppress regrowth after treatment, potentially reducing the frequency of chemical or mechanical weed control

 reduce seed and shoot production, in turn reducing the rate of spread and reinvasion.

Biological control of OMB has not been attempted elsewhere in the world.

2.3.2 Biology and pest status of old man’s beard

OMB is named for the attractive mass of fluffy seeds that persist on the plant over winter. It was introduced into New Zealand as an ornamental before 1922 and became naturalised between 1922 and 1935. It is native to Europe, where it achieves minor pest status in forests and vineyards (Mihajlovic et al., 1998). However, in Europe it never forms the vigorous thickets with massive stems that damage lowland forest fragments in many parts of New Zealand (Figure 2).

Figure 2. Old man’s beard destroying regenerating native vegetation on the Port Hills, near Christchurch. Source: Governorsbay.net.nz

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OMB is an environmental weed in New Zealand, colonising disturbed or open forests and forest margins, shrublands, riversides, cliffs, bush tracks, roadsides, hedgerows and vacant land (Gourlay et al., 2000). It is also a troublesome urban weed. OMB is adventive throughout the lowlands of New Zealand south of the Waikato (Figure 3). Auckland and Northland councils intend to keep their regions free of the weed.

Figure 3. Distribution of Clematis vitalba (and C. flammula) in New Zealand (source: Department of

Conservation.

OMB can attain a density of 7,000 stems per hectare and a fresh weight increment of 6.3 kilograms per metre per year. Stems can grow an average of 2.3 metres in 1 year, producing 20 new nodes. Plants spread both by seed and adventitious roots. West (1992) recorded an average seed fall at one site of 65 seeds per square metre per year, and estimated the life of seed in the soil to be 8–10 years. Seeds are borne on wind or water, but OMB can also spread by stem layering, and can also establish where garden refuse is dumped.

OMB is hard to kill. Control using a combination of mechanical and chemical methods can be effective but is very expensive. It is tolerant of most soils and climates. OMB is regarded as invasive in the Pacific northwest region of the USA and Canada, and in Maine and Ontario (ISSG 2017).

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OMB invades forests from the edges or from canopy gaps. The vines can grow to 20 metres in length. These can scramble over low-growing vegetation or climb into undergrowth. Vines ascend into the canopy and can climb large-diameter trees if shrubs and smaller trees provide ‘stepping stones’ to the crown. Vines can smother and collapse the forest canopy (Figure 2), leaving tall emergent trees. Curtains of OMB create dense shade, killing plants growing beneath and stopping regeneration from seedlings.

Ogle et al. (2000) found there is little regeneration even where the vine has been cleared. The number and variety of understorey trees and shrubs at a central North Island site had been severely reduced following infestation with C. vitalba, and they concluded that already-vulnerable species had been disproportionately affected by OMB. The presence of OMB had resulted in local extinction of uncommon species (Ogle et al., 2000). Based on the evidence that C. vitalba can significantly degrade tall mixed podocarp forest, C. vitalba has one of the highest weed rankings in the DOC weed database (D. Havell, DOC, pers. comm.).

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3. Information about the new organism(s)

3.1. Name of organism Identify the organism as fully as possible

Non-GMOs - Provide a taxonomic description of the new organism(s).

GMOs – Provide a taxonomic description of the host organism(s) and describe the genetic modification.

Both -  Describe the biology and main features of the organism including if it has inseparable organisms.  Describe if the organism has affinities (e.g. close taxonomic relationships) with other organisms in New Zealand.  Could the organism form an undesirable self-sustaining population? If not, why not?  How easily could the new organism be recovered or eradicated if it established an undesirable self- sustaining population? 3.1.1

Sub-class: Acari

Order: Prostigmata

Family: Eriophyidae

Genus: Aceria

Species: vitalbae (Canestrini, 1892) (http://www.faunaeur.org/full_results.php?id=94445)

3.1.2 Biology and native range

Mites are invertebrates, allied to spiders. The Eriophyidae is a family of mites that are exclusively parasitic on plants and are probably the smallest plant-feeders known (Figure 4a), sucking out plant juices from the meristematic tissues (growing points) of plants. Feeding mites transfer a substance or toxin that can cause meristems to deform. Eriophyid mites can cause a variety of symptoms, such as tumour-like galls on leaves or shoots (Figure 4b), deformities called ‘witches brooms’ on shoot tips, abnormal growth of leaf hairs (called erineum), or russetting or bronzing of leaves.

Some eriophyid species live a vagrant life on the surface of the leaf, but others feed and reproduce within complex and folded galls that help protect the population from predation and other adverse environmental conditions. These provide the immature stages of the mite with food and shelter. The development of galls is costly to the plant because it diverts resources from growth, biomass accumulation and reproduction. This often leads to the death of those parts of the plant that are galled. For example, the

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Figure 4a. Microscopically small, white, elongated gall mites on the surface of a leaf.

Figure 4b. Curled leaf and growing point deformed by a gall caused by A. vitalba after feeding for 60 days (left), and close-up of galled leaf (right) with several white mites just visible on the outside.

introduction to New Zealand in 2006 of the broom gall mite, Aceria genistae, has led to the widespread death of broom plants in some areas (Paynter et al., 2012a; Figure 5).

Gall formers are herbivores that manipulate their host plants to produce tumour-like growths. The intimate relationship between herbivore and plant that leads to gall formation requires a match between the genetics of the invertebrate that generate the right chemical signals to cause the plant to produce a gall, and the genetics of the plant that cause it to respond and produce these complex, unnatural structures (Craig et al., 1994).

This unique requirement of signal and response means that most gall-formers are specific to a single host species, and to a particular part of the plant. Gall-forming has been recorded from a wide range of invertebrate orders, but all tend to be host-specific or monophagous (Craig et al., 1994). High host

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Application Form Approval to release a new organism specificity in gall-forming species has been confirmed repeatedly in field observations and laboratory studies (Skoracka et al., 2010).

Figure 5. Gall of the broom mite, Aceria genistae (left), and wide-scale death of broom plants in Marlborough caused by broom mite (right).

Aceria vitalbae has not been recorded outside Europe. It is recorded from France east to the Balkans, as well as in Hungary, Romania, Germany, France and Italy. (https://fauna-eu.org/). Little has been recorded about its ecology in Europe, and a comprehensive review of options for biological control of OMB by Groppe (1991) noted there were only two literature references to the ecology of this species. In one of these A. vitalbae was reported to cause deformation and rolling of shoot tips and leaves of C. vitalba. Mihajlovic et al. (1998) later reported that A. vitalbae ‘caused significant damage on clematis young leaves and buds’ in Yugoslavia’. Vidovic (2016) reported that the leaf damage caused by mites in Serbia resulted in reduced fitness of OMB (especially in stressed conditions), resulting in reduced competition with other plants. Groppe (1991) also noted one statement (Buhr, 1964) reporting Clematis flammula as a host of A. vitalbae. However, this record has not been repeated by subsequent authors (including Dong et al., 2016 and the Fauna Europaea (https://fauna-eu.org/), who list C. vitalba as the sole host. It seems likely that the record is the result of a misattribution of the symptoms caused by another eriophyid mite, Epitrimerus flammulae Gerber, which is known to be specific to C. flammula (B. Vidovic, University of Belgrade, pers. comm.).

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3.1.3 Affinities with the New Zealand fauna

New Zealand has a rich mite fauna. Xue and Zhang (2008) record at least 123 species of eriophyid mites in New Zealand, including 32 Aceria species, most of which are native. All have either a single host or several reported hosts belonging to the same genus (see section 3.1.2). Manson (1984) reported that 83% of eriophyid mite species in New Zealand were capable of damaging their host plant.

No parasitoids or diseases of eriophyid mites are recorded. Eriophyid mites are so small (around 1 millimetre) that few invertebrate predators can feed on them. Mites belonging to the family Phytoseiidae are the best-known predators of eriophyid mites. Phytoseiids are considerably larger than eriophyids, and the tight, complex structures of the galls should exclude many predators while allowing most OMB gall mites to survive and reproduce safely within this refuge. However, mites moving outside the gall (Figure 4a) would be at risk from generalist predatory mites and .

McFarlane and van den Ende (1992) visited 55 sites around New Zealand and surveyed the natural enemies present on OMB. Where possible they also assessed the fauna attacking native Clematis plants growing nearby. The aims of the survey were to ensure that prospective agents were not already present in New Zealand, identify useful natural enemies of OMB that might be displaced by imported agents, and determine what parasitoids and predators were present that might hamper the development of damaging populations of introduced control agents They found that there was relatively little damage to OMB from indigenous species, and most of the damaging species were generalists. There appear to be no indigenous natural enemies of OMB that could be developed or spread around New Zealand as agents to achieve improved control. Their study also found that no native species would be displaced from OMB by the introduction of the mite (see sections 5.1.2 and 7).

Aceria vitalbae is the fourth organism (Table 1) to be considered for the biological control of OMB in New Zealand (Gourlay et al., 2000), but adequate control has not yet been achieved. Phytomyza vitalbae established readily and dispersed throughout New Zealand. Leaves are often heavily damaged, reducing photosynthetic ability, but no obvious reduction in OMB abundance has been observed. A strain of clematidina from the USA was released in 1996. Initially noticeable damage resulting from the was observed at many release sites, but a recent study found no evidence that the strain that was deliberately released is still present, and it may be extinct. The sawfly Monophadnus spinolae was released at a limited number of sites. A recent survey has found that the sawfly has established at one site near Nelson but it remains rare. Efforts are underway to establish the sawfly more widely. The stem- boring Xylocleptes bispinus has also been evaluated over many years. After consideration of recent data, this beetle was rejected as a potential agent because of the potential risk to native Clematis species.

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Table 1. Agents previously considered for biological control of OMB

Control agent Family Released Status Phytomyza vitalbae Agromyzidae 1996 Widespread, abundant Phoma clematidina Didymellaceae 1996 Extinct? Monophadnus spinolae Tenthredinidae 1998 Established but rare Xylocleptes bispinus Scolytidae Not released Rejected 2017

3.1.4 Potential for safe biological control

Why biological control? OMB causes moderate environmental and minor economic effects throughout New Zealand south of Auckland. Biological control is an appropriate tactic to apply against OMB. Once established, introduced natural enemies would colonise and damage the plant wherever it occurs, and would be widespread and persistent from year to year. Any benefits of biological control would accrue even in areas where it is not feasible to deploy other treatments.

The establishment of Aceria vitalbae would be an irreversible change. It would not be feasible to eradicate an unwanted population by the time it was detected. The agent must therefore be safe to introduce, and in particular must not:

 significantly affect populations of valued plants, whether native or non-native  significantly displace native species in their natural habitat  cause significant deterioration of natural ecosystems (see sections 3.1 and 5.1.2).

Eriophyid mites as biological control agents There is strong evidence that gall-forming eriophyid mites have narrow host ranges. Hong et al. (2001) reported that approximately 88% of eriophyid mites in China are found on a single plant species and another 10% on two species within the same genus. Only around 2% were found on plants belonging to more than one genus. Similarly, Skoracka et al. (2010) found that the hosts of 99% of 3,874 eriophyid mites assessed worldwide were restricted to a single family.

Some species are free-living on their host plants, sheltering beneath bud scales or in other plant structures. Others are able to induce their host plant to grow complex galls. Gall-forming species rely on the gall to avoid predation, shelter delicate life stages and build viable populations. Of those eriophyids capable of inducing shelter (such as the gall-forming Aceria vitalbae), 72% have a single host (Skoracka et al., 2010). This pattern of host specificity appears to hold true for species that attack Clematis. Dong et al. (2016) reported 11 species of eriophyid from Clematis species worldwide, each with a single host.

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Eriophyid mites have been used in many biological control programmes against weeds (Winston et al., 2014). Skoracka et al. (2010) and Smith et al. (2010) have pointed out that in several of these projects eriophyid mites developed on and damaged non-target plants unexpectedly in the laboratory during host- range testing. Following release, the actual field host range of several of these species has been assessed and compared with the host range revealed in lab tests. These studies confirmed that non- target plants that proved suitable for development under laboratory conditions were much less populated in the field and sustained little or no damage (Smith et al., 2010). This appears to be a particular issue for testing eriophyid species, and may be because it is easier for mites to induce galls in plant tissues in an unnatural physiological state as a result of growing in artificial conditions (Smith et al., 2010).

Predicting the host range of Aceria vitalbae in New Zealand The theory underpinning the prediction of an agent’s host range is well developed, resulting in an internationally accepted selection protocol. The ability of natural enemies to attack new hosts is strongly influenced by the evolutionary history of those potential hosts. Testing protocols operate on the premise that the species most likely to be damaged by a control agent are those closely related to the target plant. If closely related species are not susceptible, then less closely related plants won’t be either (Wapshere, 1974). Reviews of biological control practice indicate that tests using these protocols are a good predictor of subsequent field host range (Briese & Walker, 2002; Sheppard et al., 2005; Paynter et al., 2014).

Selection of plants for host-range testing The genus Clematis belongs to the sub-family Ranunculoideae of the family Ranunculaceae. There are nine native Clematis species, and four other native genera in this subfamily in New Zealand. The genus Caltha has two native species, Anemone has one, Myosurus has one, but the genus Ranunculus has 43. The phylogenetic study of Cai et al. (2009) recognised distinct groups of related genera (clades) within the sub-family Ranunculoideae. Clade I contains Clematis and Anemone, while Ranunculus and Myosurus belong to Clade II. Phylogenetically, therefore, Clematis and Ranunculus are not intimately related. Caltha is even less related. Xie et al. (2011) identified 10 recognisable clades within the genus Clematis. The Australasian species were placed in Clade III. Clematis vitalba was placed in a weak Clade VII. All of the phylogenetic analyses used placed Clade III as distantly related to Clade VII. The phylogenetic distinctiveness of the New Zealand native species accords with the unusual unisexual characteristics of the Australasian species, and with earlier sub-generic taxonomy based on morphology (Xie et al., 2011). The risk posed by A. vitalbae to plants in New Zealand was assessed by laboratory experiments. The hypothesis adopted for this study was that:

1. A. vitalbae could form galls and build thriving populations only on C. vitalba or closely related Clematis species 2. lack of attack on less-related Clematis species was sufficient to circumscribe the host range of the mite.

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If true, this would be sufficient evidence that A. vitalbae could not attack species of other genera on release in New Zealand.

The study was structured using the phylogenetic relatedness framework of Xie et al. (2011). Seven of the nine native Clematis species and a cross incorporating another were tested ((http://www.nzflora.info/search.html?q=clematis). Seedlings were sent from New Zealand to Belgrade, Serbia, for this purpose. Clematis cunninghamii could not be sourced and was not tested. Clematis marmoraria is an unusual, reduced species found in limited alpine areas of the Arthur Range in northwest Nelson. It was only available as a hybrid with C. petriei. Manaaki Whenua − Landcare Research consulted Nursery and Garden Industry NZ (now NZPPI) and growers of ornamental Clematis species for advice on which species best represent the genetic make-up of New Zealand’s commercial range of exotic ornamental Clematis species. Overall, six exotic Clematis species or hybrids were selected to represent commercial interests in New Zealand and to provide representative coverage across the 10 clades described by Xie et al. (2011). Plants were sourced in both Serbia and New Zealand.

This range of native and exotic test plants was considered adequate to test the risk to native and ornamental Ranunculaceae because:

 gall-forming eriophyids are all highly host specific (see section 3.1.2.)

 species of the same genus are much more likely to be hosts than less related plant species (Briese & Walker 2002; Sheppard et al., 2005).

Results of host-range tests

Host range tests were conducted at the University of Belgrade, Serbia (Vidovic, 2016−18). Manaaki Whenua − Landcare Research (2018a) details the methods used and the results obtained in three series of host-range tests. Series 1

Mite colonies developed only on Clematis vitalba controls and survived for 60 days on all replicates, causing serious leaf deformation (Figure 4b). No mite survival was recorded at 30 days on any of the test plants (Table 2). No mites were extracted from any of the test plants at the end of the test, and no damage to buds was observed (Figure 6). On the basis of these results (Table 2), the native species C. foetida, C. paniculata, C. quadribracteolata and C. petriei were considered to be immune from colonisation by A. vitalbae and were not tested further.

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Figure 6. Test buds of C. foetida after 60 days showing no symptoms of Aceria vitalbae attack.

Series 2

Four New Zealand native species and five ornamental species were exposed to A. vitalbae (Table 2). Unlike Series 1, mites persisted on test buds on some replicates (10% of plants for Clematis marata, C. forsteri, C. terniflora, and C. viticella; 30% of plants for C. afoliata, C. marmoraria  petriei, and C. montana; and 85% for C. stans). The number of mites in affected buds after 60 days exceeded 10, implying that mites reproduced within the buds following initial transfer. However, significant symptoms of plant damage developed only on C. stans (Table 2), where the mean severity score of 3.4 implied moderate to severe leaf deformation and shortening of internodes (Figure 7). There were no formal C. vitalba controls established for series 2, but the strong presence of A. vitalbae on C. stans (closely related to C. vitalba within Clade VII) fulfilled this role.

Series 3

The experiments completed in series 2 indicated that small populations of A. vitalbae could persist in the buds of several test plants for over 60 days without causing the leaf galls that typically developed on C. vitalba. A further series of tests examined the longer-term viability of these mite populations and the consequences of longer-term infestation for plant health. In this case, two buds were again infected with 10 mites. At 60 days the buds that had been infested were examined carefully, without damaging the infested buds. At 120 days all buds on the test plants were destructively sampled. The symptoms associated with each bud were assessed and the level of mite infestation was assessed. The species tested were the same as those tested in series 2, where these were available. The only Clematis montana plants available were hybrids.

All of the C. vitalba buds initially infested with mites survived to 60 days. All had developed leaf galls and the mean damage score was 5, the maximum score. There were more than 50 mites observed in every gall. Twelve of the 16 C. stans buds initially infested with mites remained at 60 days (Table 2). One bud contained about 50 mites, but the other 11 buds each contained approximately 10 mites. The leaves growing from the buds were twisted, and growth was reduced (Figure 7).

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Figure 7. Damage to Clematis stans buds at 60 days when initially infested with 10 Aceria vitalbae. A: infected, with symptoms; B: healthy.

. Figure 8. Retarded growth of one C. marata bud 60 days after application of mites.

Four of the 18 C. marmoraria  petriei buds initially infested with mites contained mites after 60 days. The estimated population was 10−20 mites per bud. Infestation had stopped shoot elongation. Similarly, three of 20 initially infested C. marata buds had mites at 60 days, but there were fewer than 10 mites per bud. Infestation had slowed development (Figure 8). There was no observable damage to other test plants.

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After 120 days all of the buds/growing points on the test plants and on the controls were destructively sampled and the number of mites present per bud was estimated. Every bud on the six control plants was infested, and the estimated number of mites per bud was 20−50. Every bud exhibited leaf gall symptoms (Table 2).

Six plants of Clematis stans survived to 120 days and carried a total of 84 buds. All plants had mites but only 25 of the 84 buds were infested, and the mean number of mites per bud was 3.9. The damage recorded at 60 days was no longer visible on test plants. Similarly, mites persisted on three of the native Clematis species, but the number of mites per bud had fallen to very low levels (Table 2). The proportion of buds on the test plants that were infested was also low: 5 of 102 buds for C. marmoraria  petriei, 29 of 241 for C. marata, and a single mite was found on C. afoliata. All control buds were heavily invaded.

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Table 2. Combined results of three series of experiments testing the susceptibility of Clematis species to Aceria vitalba

Clade Species Test Plants % of Mean Est. Plants % plants Mean Mean series examined plants symptom mites examined with mites symptom estimated with score at per at 120 at 120 score at mites per mites 60 days bud at days days 120 days bud (total at 60 60 buds days days examined)

VII Clematis vitalba 1 10 100% 5 20−50 2 No control - - - 3 6 100% 5 >50 6 100% 5 35 (58) VII C. stans 2 7 85% 3.4 - 3 8 75% 3.0 10−50 6 100% 0 3.9 (84) VI C. viticella 2 10 10% 0 -

V C. terniflora 2 6 17% 0.2 - X C. montana 2 10 30% 0.3 - XxVI C. montana x viticella 3 8 0% 0 0 - - - - III C. cunninghamii* No tests III C. afoliata* 1 10 0% 0 0

2 15 20% 0 3 8 0% 0 0 7 14.2% 0 0.01 (49)

III C. foetida * 1 10 0% 0 0 III C. forsteri* 2 10 10% 0

3 1 0% 0 0 - - - - III C. marata* 2 10 10% 0 3 10 30% 0.9 c.10 8 37.5% 0 0.9 (241) III C. marmoraria x petriei* 2 10 30% 0 3 9 22% 0.2 10−20 6 33.0% 0 0.6 (102) III C. paniculata* 1 10 0% 0 0 III C. petriei* 1 10 0% 0 0 C. quadribracteolata* 1 III 10 0% 0 0 II? C. 'Miss Bateman' 2 10 0% 0 Other Ranunculus sp. 3 0 - - - -

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Discussion Clematis vitalba is the acknowledged host of A. vitalbae in its native range. Clematis species are widely cultivated as ornamental species throughout the native range of the mite, yet a web search revealed no records of galls forming on other Clematis species growing in a horticultural context. The same is true of Anemone spp. and Ranunculus spp., related ornamentals that are widely grown in the home range of A. vitalbae (and which have representatives in the New Zealand flora). The host range of A. vitalbae in Europe is therefore very narrow, and probably restricted to C. vitalba. The single field record of A. vitalbae leaf galls on C. flammula (Buhr in Groppe, 1991) appears to be inaccurate (see section 3.1.2).

The narrow host range suggested by European field records was confirmed by the laboratory tests. Mites that were transferred to buds of C. vitalba controls all quickly produced leaf deformations and high populations of mites. In series 3, mites had spread and damaged all 58 buds on the control plants after 120 days. The only other test plant that produced significant leaf damage during this period was C. stans, a species closely related to C. vitalba in Clade VII (Xie et al., 2011). Even though mites established on C. stans plants, they performed poorly on this host in the laboratory. Mites were present in 30% of C. stans buds after 120 days and the mean number of mites per bud was only 3.9 (Table 1). Damage observed at 60 days was no longer discernible at 120 days. It is interesting to note that C. stans is cultivated as an ornamental in the native range of A. vitalbae but has not been recorded as a field host there. Damage on all other plant species tested was barely detectable and scored an average of less than 1, even though small numbers of mites persisted on some test plants (Table 2).

Paynter et al. (2014) examined the question whether low-level attack on a test plant in lab tests predicted its colonisation following release. They compared the performance of control agents on a test plant in lab tests with performance on controls, and used the ratio as a ‘risk score’. For weed control agents released in New Zealand they found that the probability of host use in the field was positively correlated with relative performance in lab tests. If the lab-based risk score for a plant was below 0.33, the risk of significant non-target attack on that plant in the field was low.

The mean estimated number of mites present at the conclusion of the tests in series 3 (Table 2) represents the product of oviposition success on plants and the survival of offspring. This was used to develop risk scores for four test plants. Although Aceria vitalbae completed development on C. stans (Table 2), few mites were present after 120 days, and the relative performance (risk score) was 0.11. This is below the 0.33 threshold that Paynter et al. (2014) predicted is required for a control agent to pose even spill-over risk in the field, and far below the threshold of 0.57 for full utilisation of the host in the field. Risk scores for three native Clematis species after 120 days were an order of magnitude smaller again (Table 2).

An unexpected feature of the tests was the ability of mites to persist (and presumably reproduce) on the buds of test plants without producing galls. However, in all cases numbers declined over time and populations were not viable in the long term. This was particularly evident for the native Clematis

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Application Form Approval to release a new organism species, which were either not colonised at all, or attracted low, undamaging mite numbers that declined over time. This phenomenon has been observed in other laboratory tests of eriophyid mites (Smith et al., 2010), and past test results may well have overestimated the field host range.

Eriophyid mites disperse passively on the breeze, drifting onto potential host plants. In these tests 20 adult mites were inoculated onto each bud. This is a greater colonisation pressure than would occur naturally through aerial drift. The natural frequency of colonisation in the field is likely to be lower than that induced in these laboratory tests, except perhaps in the immediate vicinity of OMB plants.

On the basis of these results, and in light of the host plant records in Europe, we conclude that:

 A. vitalbae is expected to effectively colonise only C. vitalba in New Zealand  occasional galls might be expected on exotic non-target Clematis species, especially those closely related to Clematis vitalba (Clade VII; Xie et al., 2011)  the presence of low numbers of mites is unlikely to result in damage to non-target plants.

3.2. Regulatory status of the organism

Is the organism that is the subject of this application also the subject of:

An innovative medicine application as defined in section 23A of the Medicines Act 1981?

☐ Yes ☒ No

An innovative agricultural compound application as defined in Part 6 of the Agricultural Compounds and Veterinary Medicines Act 1997?

☐ Yes ☒ No

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4. Māori engagement

Discuss any engagement or consultation with Māori undertaken and summarise the outcomes. Please refer to the EPA policy ‘Engaging with Māori for applications to the EPA’ on our website (www.epa.govt.nz) or contact the EPA for advice.

Māori views on this proposal have been sought by five routes:

1. consultation with members of Te Herenga

2. consideration of issues raised in previous similar applications

3. consideration of generic issues by an EPA reference group

4. ongoing consultation with iwi and Treaty settlement authorities in the Manawatū−Whanganui region

5. consultation with the Ngāpuhi HSNO komiti and the Ngāi Tahu HSNO Komiti.

4.1 Consultation with Te Herenga

Te Herenga, the EPA’s national network, comprises approximately 80 iwi, hapū or Māori organisation representatives with national geographical and subject-matter coverage. Information about proposed biological control of OMB was distributed to members of Te Herenga in May 2017. The announcement directed readers to the Manaaki Whenua − Landcare Research website for further detail, and invited dialogue and feedback (http://www.landcareresearch.co.nz/science/plants-animals- fungi/plants/weeds/biocontrol/approvals/current-applications/old-mans-beard). It described how the applicant intended to assess the risks, costs and benefits associated with the proposed introductions and invited members to identify any issues they would like to have addressed in the applications.

No feedback has yet been received via this route. Any issues brought to the attention of the applicant before formal consideration of this application will be made available to the EPA. Members of Te Herenga will also be specifically informed by the EPA when each application is open for public submission, and will be able to comment on how the applicant has addressed issues raised during consultation.

4.2 Issues raised in previous consultations

Three biological control agents have been introduced to attack OMB (Table 1) but applications for permission to release these species pre-date the current EPA/Environmental Risk Management Authority application regime. There are no available communications that relate directly to this proposal. However, this application is similar to other applications submitted over the last 9 years to introduce new biological control agents for weeds. Communications with Māori over previous applications are relevant here and have been summarised on the Manaaki Whenua − Landcare

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Research website (Manaaki Whenua − Landcare Research, 2018d). The key areas identified in consultations over this period are:

 possible direct effects on native plant species (see section 5.1.2)  possible indirect effects on native flora and fauna, and other valued species (see sections 5.1.2 and 5.3.2)  the need to monitor future effects (see section 7)  predictability of effects (see section 5.1.2)  specific benefits to Māori (see below)  effects on cultural and spiritual values (see below)  integration of control methods, and indigenous solutions (see below)  herbicides and biological control (see section 5.1.1)  aversion to the introduction of new organisms  lack of capacity precludes comment.  is the weed present in our rohe? (see Figure 3).

Benefits accruing to Aotearoa from the introduction of the mite or the more effective control of OMB are explained in section 5. No benefits (or costs) have been identified that are exclusive to Māori.

Manaaki Whenua − Landcare Research’s Māori plant use database lists the medicinal properties of two Clematis species, both called puawānanga or pōānanga (http://maoriplantuse.landcareresearch.co.nz/WebForms/PeoplePlantSearch.aspx). WAI 262 lists puawānanga as one of seven taonga species that were of particular significance to the claimants. The claim states that the exercise of te tino rangatiratanga o te iwi Maori ‘as it relates to indigenous flora and fauna was and is a recognition of an Iwi interest in the continued existence of flora and fauna as particular species and as interconnected threads of te ao turoa’. The Ngāi Tahu Claims Settlement Act 1998 also lists puawānanga (Clematis paniculata) as a taonga species. The introduction of Aceria vitalbae will have no direct impact on the use of these plants as natural resources or te mana o ao tūroa, because the results of host range tests indicate that no native plants will be at risk from the OMB gall mite (see section 3.1.4).

Any indirect impact of the mite through changes of relationships with other flora and fauna will be insignificant because no such interactions are expected, and because any interactions would be restricted to the immediate vicinity of OMB (see section 5.1).

The weed is of limited distribution north of Waikato, but poses a real threat to most of Aotearoa.

4.3 Māori reference group

The EPA convened a Māori reference group (MRG) to discuss the potential issues of significance to Māori relating to the proposed applications. The MRG was made up of four members with expertise and/or experience relevant to biocontrol proposals. After undertaking a review of the information available on the proposals, the MRG identified a number of initial draft principles or themes that apply

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Application Form Approval to release a new organism to biological control proposals generally (Manaaki Whenua − Landcare Research, 2018c). The following key principles were identified:

 kaitiakitanga − responsibility of Māori to manage natural resources within and beyond hapū and iwi boundaries  manaakitanga − ability of Māori to protect cultural rights and ownership within hapū and iwi boundaries  whakapapa – as the foundation for kaitiakitanga, and the need to consider the potential impacts of biocontrol agents across the breadth of trophic and ecosystem levels (see section 5.1.2)  the requirement for applicants to provide comment and/or data to evaluate potential impacts (see section 7)  the need to define the regional scope of effects, and effectively consider effects on iwi and hapū at a local level (see below)  the desirability of making vegetation restoration an integral component of biocontrol  the need to specifically address benefits to Māori − with reference to the initial draft principles, the MRG noted that the proposed introduction of these control agents might have significant direct beneficial effects on culturally valued species, and indirect benefits on the wider native ecosystem.

The MRG specifically commented that the presence of weeds of significant stature within the margins of the ngahere (forest), such as OMB, adversely affects our appreciation of the forest environment.

The focus of this application is to establish biological control of OMB to reduce large-scale environmental damage and control costs. Successful biological control would reduce the amount of herbicide currently applied to OMB (see section 5.1).

OMB is largely an environmental weed, so the benefits of successful control for Māori values, such as protection of flora and fauna, broadly align with the priorities for wider Aotearoa (see section 5.1.1). There were no benefits or costs identified that were exclusive to Māori. Benefits and costs would accrue generally to the market economy and to the environment (see sections 5.1 and 5.3).

The addition of this agent would change the fauna within hapū and iwi boundaries. However, the mite is functionally host-specific, with a low ecological footprint, and it is not expected to have an adverse impact on the functioning of ecosystems (see section 5.1.2). On the other hand, OMB is encroaching on native habitats valued by Māori, and successful biological control of the weed would stem the intensity of those effects.

4.4 Regional consultation

Horizons Regional Council of the Manawatū−Whanganui Region is the applicant, and gall mites are likely to be released in this region first. Regional and local consultation were therefore concentrated in this area.

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Information about the proposed biological control of OMB was distributed by Horizons Regional Council to iwi and Treaty settlement networks in the region in April 2017. The announcement directed readers to the Manaaki Whenua − Landcare Research website for further detail and invited dialogue to identify any issues they would like to have addressed in the application.

Two responses were received via this route, but neither was opposed to the proposal (Manaaki Whenua − Landcare Research 2018d). Any further information received before the consideration of this application will be passed to the EPA. This dialogue is expected to continue through the development of the agent and before initial releases.

4.5 Consultation with HSNO komiti No correspondence has been received during the pre-application period.

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5. Risks, costs and benefits

Provide information of the risks, costs and benefits of the new organism(s).

These are the positive and adverse effects referred to in the HSNO Act. It is easier to regard risks and costs as being adverse (or negative) and benefits as being positive. In considering risks, cost and benefits, it is important to look at both the likelihood of occurrence (probability) and the potential magnitude of the consequences, and to look at distribution effects (who bears the costs, benefits and risks).

Consider the adverse or positive effects in the context of this application on the environment (e.g. could the organism cause any significant displacement of any native species within its natural habitat, cause any significant deterioration of natural habitats or cause significant adverse effect to New Zealand’s inherent genetic diversity, or is the organism likely to cause disease, be parasitic, or become a vector for or plant disease?), human health and safety, the relationship of Māori to the environment, the principles of the Treaty of Waitangi, society and the community, the market economy and New Zealand’s international obligations.

You must fully complete this section referencing supporting material. You will need to provide a description of where the information in the application has been sourced from, e.g. from in-house research, independent research, technical literature, community or other consultation, and provide that information with this application.

The potential risks, costs and benefits of the proposed introduction to New Zealand of Aceria vitalbae have been identified by literature review, by reviewing the issues raised in previous applications to ERMA/EPA to introduce biocontrol agents for weeds, and by consultation with stakeholders. All effects identified during this process are listed on the Manaaki Whenua − Landcare Research website (Manaaki Whenua − Landcare Research, 2018b). Those effects considered to be potentially significant are highlighted on that list, and only those effects are addressed in detail here (section 5). Potential effects are associated with

 permanent establishment in New Zealand of the OMB leaf-galling mite (A. vitalbae)

 reduction in the abundance and vigour of existing OMB infestations

 reduction in the spread of OMB.

5.1 Potential effects on the environment

5.1.1 Potential beneficial effects on the environment

The introduction of the mite would benefit the environment if galls caused sufficient suppression of OMB to:

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 reduce its current adverse effects on native species, partially restoring plant and animal biodiversity and ecosystems

 limit the rate at which such infestations establish damaging infestations

 limit the frequency of herbicide application, the incidence of non-target herbicide damage, and pesticide loads in the environment.

Could the control agents reduce the displacement of native species by OMB infestation?

OMB can threaten biodiversity values in a wide range of habitats and ecosystems (e.g. Ogle et al., 2000; see section 2.3.2). Left uncontrolled, OMB vines produce dense, permanent masses of foliage that can dominate, replace and physically destroy a plant canopy. Vines growing across the ground cast shade that can prevent regeneration (see section 2.3.2). These adverse effects can be managed at critical sites, but conventional control is difficult, expensive, and often impossible (Manaaki Whenua − Landcare Research, 2018e).

Biodiversity group: … looks after a wide range of high value habitats, including wetlands, bush remnants and dune lakes. They control a range of pests in these areas … The annual spend on OMB would be between $20–40 … thousand dollars.

Horizons has some large outstanding natural features, such as the Manawatu Gorge, Taihape high country, Volcanic plateau, Makuri Gorge, Ruahine and Tararua ranges and many large rivers including the Manawatu and Rangitikei. All of these areas have high ecological, recreational and economic values attached to them … Given time, OMB will take over and destroy the forests, riparian margins and wetlands which are associated with these locations. The Manawatu and Makuri gorges, Rangitikei river gorge, Manawatu river and other landscape features are already heavily infested with OMB, and work is being done to prevent this damage from occurring in the other locations

(Jack Keast, Environmental Management, Horizons Regional Council)

… river valleys when deciduous trees lose their leaves and the mass of OMB vines becomes more obvious these [landscape] values are degraded. OMB can modify the environment so much that others weeds can establish in situ and impede access to waterways and other environs … Council supports community initiatives like Project Devine, and other local groups with limited inputs. Reserves Department and Engineering Riverworks engage contractors.

(Robin van Zoelen, Biosecurity Officer, Tasman District Council)

Galls created by eriophyid mites eventually age, dry out and turn woody. When these galls are large, shoots can die back and snap. This is the case for the closely related broom gall mite, Aceria genistae, which was released in New Zealand in 2008. It produces woody galls and is now causing serious damage to broom populations in parts of the South Island, restoring hill country vegetation

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(Figure 5; see http://www.landcareresearch.co.nz/publications/newsletters/biological-control-of- weeds/issue-75/broom-gall-mite-a-decade-on).

Similar symptoms have been observed on OMB attacked by A. vitalbae in Serbia (B. Vidovic, University of Belgrade, pers. comm.). Galling of stems in New Zealand would slow the accumulation of OMB biomass in the forest canopy and reduce the rate of growth of vines on the ground. Where galling is heavy there is likely to be stem die-back and the death of plants. Significant die-back would limit the ability of OMB to compete for light and space in vulnerable habitats, allowing native species to regenerate and partially restoring biodiversity values. The benefits of successful control to the environment are likely to be minor to moderate. However, it remains uncertain whether that level of control will be achieved.

Could the control agent reduce the spread of OMB and limit future harm to populations of native organisms?

Although OMB is distributed widely in New Zealand, it does not occupy all available habitats within that range. It occurs rarely north of Waikato, and in some regions its distribution is limited, and those regional councils work to contain OMB within its existing range to protect the rest of the region. Where OMB is abundant, regional councils often take action to protect areas of high biodiversity value (Manaaki Whenua − Landcare Research, 2018e). Restricting the dispersal of OMB therefore remains important even though it is widespread and abundant.

Successful biological control is likely to lower the rate of OMB invasion into areas of high biodiversity value, and that benefit is likely to be minor to moderate. Every gall would hamper shoot growth, reducing the rate at which vines spread into new canopy and reducing the amount of seed produced by the affected stem. Heavy galling would cause stem die-back, thinning the OMB canopy and reducing seed production. Successful control of OMB would reduce the likelihood of OMB seeds dispersing to colonise Auckland and Northland, establish new sites within its existing range, or reinvade sites where OMB management has achieved local eradication.

Gall mites float in the breeze and would colonise and challenge newly established OMB plants in vulnerable or novel habitats. Death of founding plants would limit the rate of establishment of new OMB populations.

Could biological control reduce the adverse effects of current or future use of herbicides?

Greer and Sheppard (1990) described how OMB is routinely controlled, usually by cutting vines and spraying regrowth at ground level. In extreme infestations the OMB canopy is sprayed by helicopter. The use of herbicides for OMB control can result in significant non-target impacts in native habitats, and conventional control techniques may be as damaging to a site as the weed itself (Ogle et al., 2000).

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Successful biological control of OMB would reduce the impact of OMB and give land managers the option of living with the weed instead of applying herbicide. Successful biological control is likely to reduce the vigour of OMB to a state where it is no longer necessary to undertake management actions that are in themselves detrimental to biodiversity values. As helicopter operations are relatively rare, and as ground-based application of herbicide can normally be used without damage to native vegetation, the environmental benefits of reduced herbicide use are probably minimal to minor. However, the potential economic benefits resulting from reduced herbicide use are large (see section 5.3.1).

In summary, OMB is a weed of considerable significance in natural areas of New Zealand (Manaaki Whenua − Landcare Research, 2018a) and is difficult to manage. Successful biological control is likely to produce minor to moderate environmental benefits. It remains uncertain whether the release of A. vitalbae will result in successful biological control, and partial control would have fewer environmental benefits. The economic benefits of successful control in reserved areas are considered in section 5.3.1.

5.1.2 Potential adverse effects on the environment The establishment of the OMB gall-forming mite in New Zealand would have adverse effects on the environment if:

 feeding on non-target species reduced populations of any native plant

 the introduced mite interfered significantly with trophic webs.

Biological control of OMB would have adverse effects if it:

 facilitated the establishment of worse weeds.

Does Aceria vitalbae pose a risk to native plant populations?

Aceria vitalbae is widely distributed in Europe (see section 3). Ranunculus and Anemone, two genera represented in the native New Zealand flora, have been cultivated in Europe as ornamentals (Groppe, 1991) for centuries. The symptoms of attack by A. vitalbae are dramatic (Figure 2), yet have never been recorded in ornamental Ranunculus or Anemone species in Europe. Similarly, despite a long history of cultivation of ornamental Clematis in Europe, there are no published or web records of galls that might be attributable to A. vitalbae on species other than C. vitalba. The single record on C. flammula appears to be a misidentification (see section 3.1.2).

The host range of A. vitalbae was examined experimentally in Serbia, and the results are presented and discussed in section 3.1.4. The narrow host range suggested by European field records was confirmed by the laboratory tests. A heavy load of 20 adult mites was applied to the vegetative buds of the test plants. Those transferred to buds of C. vitalba controls all produced leaf deformations and high populations of mites. Clematis stans supported mite populations for a time, but no galls formed

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The mites applied to most New Zealand native Clematis sp. did not persist at all. Mites were observed on several native species, but at very low numbers, and damage was barely detectable (section 3.1.4).

Host range tests support the view that the mite is functionally specific to C. vitalba. The risk to native flora is considered to be minimal because:

 gall-forming herbivores are usually highly specific to one or a few host plants (Craig et al. 1994)  gall-forming eriophyid mites are highly host-specific ( see section 3.1.2)  A. vitalbae appears to be specific to OMB in its native range (see section 3.1.2)

We conclude that A. vitalbae is expected to colonise only C. vitalba in New Zealand. However, occasional galls might be expected on exotic non-target Clematis species, especially those closely related to C. vitalba (Clade VII; Xie et al., 2011). However, it is improbable that the OMB leaf-galling mite would cause significant damage to populations of native plants in New Zealand.

Could the agents indirectly cause significant changes in the relationships between native species?

The introduction of the mite could adversely affect existing ecosystem relationships if predation or of this new host resulted in significant population changes in other native species.

‘Apparent competition’ between two species occurs when both are preyed upon by the same natural enemy. For example, if species A and species B are both prey for a predator or parasitoid, an increase in the population of species A could lead to an increase in overall prey numbers, followed by an increase in predator or parasitoid numbers, which in turn could exert disproportionate pressure on populations of species B. The introduction of a control agent would cause such adverse effects on trophic webs if populations developed that generated apparent competition in sensitive habitats, leading to significant displacement of valued native species.

A trophic web is the notional representation of all of the biotic interactions affecting the population of a single species, in this case interactions between biocontrol agents and potential parasitoids, predators, and diseases. Few trophic webs have been adequately described anywhere (but see http://www.landcareresearch.co.nz/publications/newsletters/biological-control-of-weeds/issue-69/food- web-inside-broom-galls). It is therefore not possible to precisely define the effect of introducing a new organism to such a web. Kaser and Ode (2016) point out that trophic webs are complex, and that signs and strengths of interactions between elements of trophic webs can be difficult to measure or predict. Frago (2016) and Kaser and Ode (2016) also point out that habitat complexity and

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Despite these reservations, the relative importance of OMB gall mite in web dynamics can be inferred from the biology and ecology of the agent and the target weed, as follows.

 The mites are minute and will represent insignificant biomass in the ecosystem. If the agent fails to establish, or does not achieve high population levels following release, it is unlikely that its presence could become a key factor in any trophic web.

 The agent is host specific (see section 5.1.2) and will only reach high populations in the immediate vicinity of OMB plants.

 Eriophyid mites do not appear to have parasitoids that might mediate apparent competition.

 Most eriophyids will develop deep within the gall and escape the attention of many predatory mites. Any increase in predator populations resulting from feeding on the gall mite will be restricted to the habitat immediately surrounding the galled OMB.

 Although OMB is widespread (Figure 3) and can be abundant, it is not everywhere. Interactions will be localised to OMB infestations.

 OMB itself is an ecosystem modifier, and is likely to be a growing influence on trophic webs within infested sites, outweighing any effects the control agents might have.

Biological control aims to reduce the physical dominance of OMB and its influence on trophic webs.

Little can be said about other potential trophic interactions, such as common diseases, but any apparent competition will be restricted to where the control agents are abundant – the vicinity of OMB infestations. Given the available information, Manaaki Whenua − Landcare Research concludes that Aceria vitalbae is unlikely to significantly influence the quality of trophic webs outside OMB infestations. Successful biological control would progressively reduce any influence of the agents on trophic webs and would also partially reverse the effects of OMB itself.

Could biological control of old man’s beard lead to infestations of worse weeds?

Successful biological control is not expected to lead to replacement with a worse weed, for the following reasons.

 OMB vines can form massive curtains that shade out or break underlying vegetation (see section 2.3.2). It is unlikely that any other vine could be more effective then OMB at displacing flora and fauna in forest habitats.

 Other weedy vines are not as widespread or abundant as OMB, and do not necessarily co- occur with OMB. Even if replacement occurred, the benefits of OMB control at the many sites where there was no replacement weed (see section 5.1.1) would exceed the costs incurred at the few sites where a worse weed replaced OMB.

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 OMB can grow on the ground and smother underlying vegetation. There are many other weeds of disturbed areas that could also fill this role, but it is unlikely that the effects of any of these would be worse than OMB.

No other potential adverse effects on the environment were considered significant (Manaaki Whenua − Landcare Research, 2018b). Few native invertebrates use OMB at present (see section 3; Mcfarlane & van den Ende, 1992) so reduction in the abundance or biomass of OMB would have no direct effect on any native invertebrate species.

Any effects of the gall mite on OMB abundance will develop gradually, and no catastrophic or rapid changes to invaded habitats are expected.

5.2 Potential effects on human health

5.2.1 Potential beneficial effects on human health There would be no significant benefit for human health in New Zealand from the establishment of the gall mite or from the successful control of OMB. Successful biological control may limit the future use of herbicides for OMB control, but any benefit for human health is tenuous, as relatively little herbicide is currently applied for OMB control in New Zealand (see section 5.3.1).

5.2.2 Potential adverse effects on human health Neither the establishment of the gall mite nor the successful control of OMB would have significant adverse effects on human health in New Zealand. The mite is minute and does not bite or sting. A PubMed search did not reveal any evidence that eriophyid mites cause allergic reactions.

A brief search of the internet suggested that extracts of Clematis have pharmacological potential (e.g. http://agroweb.org/?id=11&l=1531&ln=en&url=clematis-vitalba-the-travellers-joy-unknown-benefits). Successful biological control would reduce the incidence and biomass of OMB in the environment but not enough to eliminate any future use as a source of phytochemicals.

5.3 Potential effects on the market economy

5.3.1 Potential beneficial effects on the market economy Successful biological control of OMB would benefit the market economy if populations of the gall mite reduced control costs for land managers, regional councils, DOC, occupiers and other entities that manage land.

OMB imposes costs on many organisations. It was not possible to gather a current estimate of overall control costs, but a description of the costs obtained from some of the affected organisations during pre-application consultation is presented here, followed by an explanation of how the OMB gall mite could help to mitigate those costs.

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Regional councils and territorial authorities

OMB affects the biodiversity values of regional reserves and the amenity values of rivers and parks in many regions. It is also a major nuisance for rate-paying householders. OMB features in the Regional Pest Management Plans (RPMP) of 15 regional councils and territorial authorities (http://www.biosecurityperformance.maf.govt.nz/). Plans outline how councils manage a weed and impose requirements (costs) on occupiers to manage weeds on their own properties:

Residents in the Rangitikei district are rated a target rated for funding specifically used to control OMB. This rating gathers $95,000 per year, and Horizons also puts 200 staff hours to this, at a total cost of around $17,000. This money goes to fund a community group called the Rangitikei Environment Group (REG). REG works to control OMB throughout the district on public and private land. Jack Keast, Environmental Management, Horizons Regional Council

OMB is relatively uncommon or absent from six regions, including Northland, Auckland and Waikato (Figure 3). These regions invest in surveillance, education, eradication and containment to ensure that OMB never becomes a problem there:

… we currently have about 200 known sites … staff and contractors spend roughly 700 hours per annum on the control of OMB, which is done through spraying and cut and pasting stems. Roughly $25 000 is spent on external contactors per year and costs are increasing

Hamish Hodgson, Waikato RC

Greer and Sheppard (1990) reported that in the three financial years to 1989/90, the local authorities surveyed together spent $145,000, $143,000 and $205,000 per annum to manage OMB. Regional, unitary and district councils have continued to invest in the management of OMB in their areas since then. Five regional councils recently provided estimates of their current expenditure on OMB management. For these regions alone, expenditure totalled approximately $760,000 annually (Manaaki Whenua − Landcare Research, 2018e). This underestimates national expenditure by local authorities because other regions also invest in OMB management, and district councils also undertake control.

OMB is a major plant pest in our region both in the Northern (Taihape) and Southern (Turakina) areas and grows in such inaccessible locations we believe the long term control/containment of this pest plant can only be achieved by biological controls … Our region’s current control measures for the containment of OMB is lessening the impact of this pest plant in our urban and rural areas; however, in the long term the use of significant amounts of agrichemicals in sensitive environments will need to be closely watched and controlled. The use of biological controls, such as the mite, will be a much more cost-effective solution. Ross McNeill, Chief Executive, Rangitikei District Council

Cost for OMB control in Tasman District. Project Devine $255,000, this costing is only for OMB control, Upper Buller Catchment $20,000, Riverworks $30,000, Reserves $15,000, project $6,000. Total $326,000. Robin van Zoelen, Biosecurity Officer, Tasman District Council

HRC Pest plant Team OMB budget 2016–2017: $126,750. This is our current spend for OMB control throughout the region. Our current RPMP has areas where we do and do not undertake OMB control, so

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this money only reflects what we spend in our priority areas. To actually control OMB over the whole region would be magnitudes more money, and probably physically impossible with current techniques … HRC River Management Group …’soft engineering’ including tree planting… All these plantings are at risk from OMB, as they can be pulled down by OMB, rendering them ineffective as flood or bank protection. Currently there are a lot of plantings along the rivers which are being negatively impacted by OMB … The River Engineering Group spend between $20 – 40 thousand dollars per year. Jack Keast, Environmental Management , Horizons Regional Council

Department of Conservation

The adverse effects of OMB on biodiversity values are most evident in the natural estate. There is no market value established for native forest in New Zealand. When the biological control programme against OMB was first established, Greer and Sheppard (1990) used ‘contingency valuation’, a non- market valuation technique, to estimate what the community would be willing to pay for research leading to successful control of OMB. They surveyed 3,000 members of the public with a 46.1% response rate. The community appeared willing to pay $44−$111 million to achieve this. While the public’s investment might be different now, this result reflects the public antipathy towards OMB, which is often a nuisance plant in backyards and peri-urban areas.

Greer and Sheppard (1990) also reported that in the three financial years to 1989/90, DOC spent $332,000 to $555,000 per annum to manage OMB. DOC continues to invest in OMB management to maintain the biodiversity values it is required to protect.

Over 120 conservation units have C. vitalba records, and there are at least 47 infestations where some form of monitoring and control have occurred. Infestations range from zero density, lightly infested, widely scattered, to common and abundant with up to 75% cover. Sites are known in estuaries, cliffs, offshore islands, grassland, forest, shrubland and riverbeds. Eradications and containment programmes are progressing at some sites. While some sites have been reduced to zero density, some programmes initiated in the 1990’s are still active, sites of C. vitalba in 1990 still had pockets of C. vitalba in 2016. D. Havell, Department of Conservation

QEII National Trust

The Queen Elizabeth II National Trust (QEII National Trust) covenants land with owners, and these covenants are managed for their ‘open space’ values. Many have OMB recorded within them. Weed control within covenants is largely undertaken by land owners and partner agencies, with advice from QEII (Gareth Eloff, QEII National Trust, pers. comm.). In the Horizons region alone this includes parts of approximately 104 covenants, 30−50% of all registered covenants.

Many farmers have good intentions, but investing in weed control on non-productive land can fall low on their priority list. Control measures are expensive and must be repeated. For example, in one covenant $22,100 was spent on control over 103 hectares during 2013−2015 ($71.50 per hectare per year), and $10,500 was spent on control over 59 hectares in 2016/17 ($89 per hectare per year) (G. Eloff, QEII National Trust, pers. comm.).

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This will get worse as waterways are fenced off to help with water quality and OMB spreads to these areas. There are still areas of Tararua it hasn't got to yet but it will eventually … Currently I have recorded it in 35% of covenants but [it] is likely that it could already be in 50%. The way it has spread in the region over the last few years I would expect it to possibly be in 90% by another 10–20 years … Many have good intentions but farmers are generally time poor and controlling OMB normally never makes it above the bottom of the list for most … In broken terrain, especially areas with steep banks and deep gorges, control is difficult. The broken terrain provides plenty of light for it to establish and it loves scrambling up banks re- rooting where it touches the ground all the way up. The broken terrain also makes getting around to find and control extremely time consuming. Some larger covenants with steep broken terrain are just not economic to control ... With the amount of seed in the landscape and re-infestation one of the main troubles with control is that is not just a one-time hit. It is currently perpetual … Any biological control has to be a help, and for much of the region and many of the covenants … [this is] probably the only hope long term. excerpts from QEII field staff responses

Forestry and other stakeholders OMB vines impede both productivity and operations in production forests. OMB is controlled in the farmed landscape by a competitive pasture sward and by sheep and cattle browsing. Withdrawal of grazing in areas where OMB is present results in almost immediate invasion. Livestock are normally excluded during the establishment of new forests, allowing OMB to establish. Following harvest, bare ground and slash provide an ideal nursery environment for OMB seedlings. A forest company near Wanganui had to respray and replant a second rotation compartment due to OMB, while a Taihape- based farm forester would not replant because OMB affected tree quality (C. Davey, Horizons Regional Council, pers. comm.). OMB appears to have a tolerance to Terbuthylazine, a herbicide used to provide long term suppression of competing weeds in forests. This allows OMB to establish adjacent to forest seedlings (Figure 9), which it can climb and smother, reducing yields (A. Gordon, NZ Farm Forestry Association executive member, pers. comm.). OMB impedes access for silvicultural work, and the risk to workers felling trees bound up with OMB imposes health and safety-related costs at harvest (R. van Zoelen, Biosecurity Officer, Tasman District Council, pers. comm.).

…There is no exotic forest species that is currently grown in NZ that can outgrow OMB and so without a very effective biocontrol much of our current forest estate will be eventually compromised…. many forests will be unable to re-establish without extremely costly and environmentally unfriendly chemical control strategies targeting OMB.

A. Gordon, NZ Farm Forestry Association executive member and farmer

Private land owners incur costs for shelter belt management on farms and orchards and when restoration work is implemented to restore native habitats. Successful biological control would reduce these costs. However, although real and substantial, the size of these potential benefits is unclear.

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Figure 9. OMB vines growing up a young tree.

In summary, at least one million dollars is being spent annually by occupiers, councils, DOC and other organisations to manage the adverse effects and spread of OMB. Much of this sum is spent on herbicide application. In summary, it is highly likely that successful biological control of OMB would reduce the frequency and cost of herbicide use, and could eventually result in policy changes removing the mandatory requirement (in some situations) for occupiers to control OMB. This would lead to reduced control costs for regional councils, DOC, occupiers and other entities managing land, with minor to moderate benefits to the market economy. Actual potential benefits are difficult to predict because it remains unclear what level of control will be achieved. Lower levels of control would achieve lower benefits.

5.3.2 Potential adverse effects on the market economy The introduction of Aceria vitalbae would have adverse effects on the market economy if it:  damaged non-target plants enough to reduce the usefulness of valued ornamental species, making sale in nurseries unprofitable  vectored viral diseases.

Could the introduction of the mite adversely affect ornamental plants? The establishment of the gall mite would have adverse effects on New Zealand’s market economy if damage to non-target plants significantly reduced the persistence of valued ornamental species in gardens, making their sale in nurseries untenable.

Section 3.1 describes tests designed to assess the susceptibility of a range of Clematis species, including species on which the development of new ornamental cultivars has been based (also see

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Application Form Approval to release a new organism section 5.1.2). The NZPPI helped select for host range testing in Serbia Clematis species from which commercial varieties hae been developed (see section 3.1.4). Although not all of the plants they suggested could be sourced in Serbia, none of the species tested was susceptible to A. vitalbae (see section 3.1.4). The tests were sufficiently robust to show that there is no significant risk to ornamental Clematis species from the gall mite.

Aceria vitalbae is widely distributed in Europe (see section 3). Ranunculus and Anemone, two genera represented in the native New Zealand flora, have been cultivated in Europe as ornamentals (Groppe, 1991) for centuries. The symptoms of attack by Aceria vitalbae are dramatic (Figure 2), yet have never been recorded in ornamental Ranunculus or Anemone species in Europe. As these species are not hosts of A. vitalbae in Europe, native species will not be susceptible in New Zealand. Although there are no records of A. vitalbae persisting on non-target clematis species in Europe, host- range tests could not rule out the possibility that the mite might be found occasionally on exotic species other than C. vitalba. However, persistence of the mite in tests was low, and it is highly unlikely that A. vitalbae populations would grow to cause significant damage to ornamental Clematis species, and the risk to the market economy is therefore minimal.

Could old man’s beard gall mites vector viruses that are damaging to other plant species?

Viruses are mostly vectored by insects such as aphids and leafhoppers, and relatively few are known, or even suspected, to be vectored by mites. However, of those that are, all are transmitted by eriophyids. Stenger et al. (2016) note that approximately 4,000 eriophyid species are known, but the actual number is likely to be at least five times that. Of those eriophyids, the number known to carry viruses is small. Eleven eriophyoid species have been proven or suspected to transmit viruses (Table 18.1; Stenger et al., 2016). Stenger et al. noted that although transmission is thought to be semi- persistent in some examples, the acquisition, retention and inoculation periods of viruses in eriophyids are poorly known. Several of these viruses are economically important.

The introduction of A. vitalbae would have adverse effects if it led to:

 increased transmission of resident viruses in economically important crops

 the introduction and transmission of virus strains to ornamental Clematis species, or other economic plants

 the introduction and transmission of viruses to native Clematis species.

A literature search found one virus closely associated with Clematis in the USA (http://www.genome.jp/dbget-bin/www_bget?refseq:NC_033777), but none in Europe. Grower-related websites and blogs were consulted. None highlighted viruses as significant diseases of ornamental Clematis growing in Europe. A number of viruses that have a wide range of plant hosts have also been isolated from Clematis species in Europe, including cucumber mosaic virus, tobacco rattle virus, tobacco streak virus and tomato bushy stunt virus (Rana et al., 1987). The vectors for these viruses

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Application Form Approval to release a new organism are various (passive, mechanical, aphids, nematodes, seeds, leafhoppers) but none are among the 11 viruses known to be vectored by gall mites (Stenger et al., 2016).

The serious phytoplasma disease of grapes Flavescence dorée has recently been isolated in plants growing around infected European vineyards, including Clematis vitalba (https://link.springer.com/article/10.1023/B:EJPP.0000015361.95661.37), but the vector for this disease is a leafhopper, not a gall mite (https://link.springer.com/article/10.1007%2Fs13593-014-0208- 7).

It is unlikely that the introduction of A. vitalbae will introduce any plant disease to New Zealand or will vector any resident viruses because:

 there do not appear to be any Clematis-specific viruses that could be introduced from Europe with the mite

 important diseases in Clematis in Europe are not vectored by gall mites

 the OMB gall mite is host-specific (see section 3.1.4), and the likelihood of persistent feeding on any plant other than Clematis species is low, so it is improbable that it could vector viruses between plants outside the genus Clematis

 OMB gall mites have limited ability to actively migrate between plants, which will limit their ability to carry viruses, not only between host species but even between OMB plants

 rearing for several generations in containment on disease-free New Zealand OMB will further reduce any residual risk of associated pathogens.

5.4 Potential effects on society and communities

5.4.1 Potential beneficial effects on society and communities

Successful biological control of OMB would have benefits to societies and communities if:

 replacement of OMB with other vegetation following successful biological control leads to improved public conservation values  successful biological control results in better use of conservation volunteers and community resources.

Other than those already highlighted in section 5.1.1, no significant benefits to society or communities from biological control of existing OMB infestations were identified. Successful control is likely to limit the future importance of OMB as an environmental weed and reduce the need for investment of community resources and conservation volunteers in OMB management.

5.4.2 Potential adverse effects on society and communities The introduction of the gall mite would have a significant adverse effect on society and communities if:

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 control of OMB reduced the ornamental value of ornamental species currently growing

 Aceria vitalbae caused a public nuisance.

Section 3.1 describes tests designed to assess the susceptibility of a range of Clematis species, including those from which some new ornamental cultivars have been developed. None of these species sustained populations of A. vitalbae and no damage was evident. It is therefore improbable that A. vitalbae will cause significant damage to ornamental Clematis species, and the risk to ornamental clematis already growing in New Zealand gardens is therefore minimal.

Adult gall mites are less than 1 millimetre long and will only be abundant on or near OMB plants. Mites cannot fly, but they do disperse on the wind. One paper noted that 16% of mites extracted from Brazilian curtains were eriophyids, but no adverse consequences of that were recorded. There is no record of eriophyid mites causing human health concerns (see section 5.2.2). It is improbable that the gall mites will cause a public nuisance.

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6. Pathway determination and rapid assessment

Under sections 38I and 35 of the HSNO Act your application may be eligible for a rapid assessment. The pathway for your application will be determined after its formal receipt, based on the data provided in this application form. If you would like your application to be considered for rapid assessment (as per the criteria below), we require you to complete one of the below sections. Fill in the section that is relevant to your application only.

6A. New organism that is or is contained within a veterinary or human medicine (section 38I)

6.1. Controls for organism

Describe the controls you propose to mitigate potential risks (if any). Discuss what controls may be imposed under the ACVM Act (for veterinary medicines) or the Medicines Act (for human medicines)

Not applicable

6.2. Discuss if it is highly improbable (after taking into account controls if any):

 The doses and routes of administration of the medicine would have significant adverse effects on the health of the public or any valued species; and  The organism could form an undesirable self-sustaining population and have significant adverse effects on the health and safety of the public, any valued species, natural habitats or the environment Do not include effects of the medicine or new organism on the person or animal being treated with the medicine

Not applicable

6B. New organism (excluding genetically modified organisms) (section 35)

6.3. Discuss if your organism is an unwanted organism as defined in the Biosecurity Act 1993

Aceria vitalbae is not listed in the Ministry for Primary Industries Unwanted Organisms Register (https://www1.maf.govt.nz/uor/searchframe.htm)

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6.4. Discuss if it is highly improbable, after taking into account the proposed controls, that the organism after release:

 Could form self-sustaining populations anywhere in New Zealand (taking into account the ease of eradication)  Could displace or reduce a valued species  Could cause deterioration of natural habitats,  Will be disease-causing or be a parasite, or be a vector or reservoir for human, animal, or plant disease  Will have adverse effects on human health and safety or the environment

6.4.1 Risk of unwanted populations It is very unlikely that the agent could be successfully eradicated once established, so release into the New Zealand environment should be considered as irreversible (section 3.1). The object of introducing Aceria vitalbae is to establish desirable self-sustaining populations wherever OMB infestations exist in New Zealand. This species would only be considered undesirable if it adversely affected valued native plants or ecosystems. Aceria vitalbae is not expected to have significant adverse economic or environmental effects in New Zealand (see sections 3.1.4, 5.1.2, 5.4.2). Given the potential benefits of the introduction, no populations of A. vitalbae are expected to be unwanted.

6.4.2 Risk of displacement of valued species Significant displacement of valued species is considered improbable for the following reasons.  The evidence presented in sections 3.1.4 and 5.1.2 indicates that native plant species are not at significant risk of attack by A. vitalbae.  Valued exotic plant species are not at significant risk from this mite either (sections 3.1.4, 5.3.2).  It is improbable that any native plant or invertebrate species would be significantly displaced (section 5.1.2). There appears to be no native invertebrate species commonly associated with OMB that could be significantly displaced by A. vitalbae (McFarlane & van den Ende, 1992).  Any change in OMB abundance resulting from biological control is likely to be gradual, over years. It is highly improbable that this control agent will cause catastrophic decline in any OMB infestation that might then lead to widespread rapid change in any native habitat. Successful biocontrol will tend to restore affected habitats (Figure 2) to a pre- invasion state over time.  Permanent reductions in OMB biomass could theoretically result in replacement in existing sites by equally or more damaging invasive species (see section 5.1.2). This potential effect is not considered significant because it is unlikely that those weeds would be any more damaging than OMB in affected habitats. In native habitats OMB is more likely to be displaced by native species. Any effect is likely to be variable from place to place.

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6.4.3 Risk of deterioration of natural habitats Founding populations of A. vitalbae will be relatively small, and it will take several years before the density of galls on OMB reaches damaging levels. OMB plants are perennial, with significant reserves. Suppression of growth or deterioration of vines will be gradual, and it is unlikely that the control agents could kill a plant within a single season. Change in OMB biomass and abundance will therefore be gradual, allowing surrounding vegetation time to regain the space occupied by OMB. Deterioration of natural habitats is therefore highly improbable.

6.4.4 Risk of carrying disease Aceria vitalbae does not form diseases in its own right, and is not parasitic on vertebrates. Some eriophyid mites are acknowledged vectors of plant viruses. However, A. vitalbae is not expected to be a significant vector or reservoir of plant diseases (see section 5.2.1). As the agent is expected to occur almost exclusively on OMB, any transmission risks to other species in this genus are further reduced.

6.4.5 Risk of adverse effects on human health A short literature search (PubMed) revealed no records of eriophyid mites implicated in adverse effects on human health. The effect of eriophyids on humans was not treated in the review of new literature by de Lillo and Skoracka (2010). No credible mechanism for adverse effects of OMB mite on human health and safety has been suggested.

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7. Other information

Add here any further information you wish to include in this application including if there are any ethical considerations that you are aware of in relation to your application.

This application raises no known ethical considerations.

7.1 Post-release monitoring and measurement of impact

The development of biocontrol for OMB is supported by the National Biocontrol Collective. The collective has stated its commitment to the evaluation of target and non-target effects of biological control agents when this is appropriate (http://www.landcareresearch.co.nz/__data/assets/pdf_file/0005/83318/Basics_National_Assessment_ Protocol.pdf). Manaaki Whenua – Landcare Research will provide populations of the control agent to regional councils and other organisations, and will oversee agent release and immediate follow-up. Monitoring will be done on a hierarchical basis. Initially, signs of establishment will be determined by visually searching for galls on OMB plants growing near the release sites. Presence of control agents on non-target plants will also be recorded. If galling of OMB plants becomes extensive and impacts are suspected, the Collective will then initiate measurements of the mite’s dispersal and effects over time. 7.2 Wider monitoring of biological control in New Zealand

Manaaki Whenua – Landcare Research is focused on constant improvement in the biological control of weeds practice in New Zealand, including world-leading research into minimising the interactions of introduced agents with existing trophic webs (Paynter et al., 2010; Fowler et al., 2012), better prediction of success (Paynter et al., 2012b), how agents disperse (Paynter & Bellgard 2011), the accuracy of host range testing in predicting eventual host range following release (Paynter et al., 2014), and monitoring the safety of biological control in New Zealand (Paynter et al., 2004).

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8. Checklist This checklist is to be completed by the applicant

Application Comments/justifications All sections of the application form completed ☒ Yes ☐ No or you have requested an information waiver (If No, please discuss with an under section 59 of the HSNO Act Advisor to enable your application to be further processed)

Confidential data as part of a separate, ☐ Yes ☒ No N/A identified appendix

Supplementary optional information attached:

 Copies of additional references ☒ Yes ☐ No

 Relevant correspondence ☐ Yes ☒ No See Manaaki Whenua Landcare Research website

Administration Are you an approved EPA customer? ☒ Yes ☐ No Fee paid If Yes are you an: Applicant: ☒ Agent: ☐

If you are not an approved customer, Fee paid payment of fee will be by:  Direct credit made to the EPA bank ☒ Yes ☐ No account (preferred method of payment) ☐ Payment to follow Date of direct credit:

 Cheque for application fee enclosed ☐ Yes ☒ No ☐ Payment to follow

Electronic, signed copy of application e- ☒ Yes mailed to the EPA

Signature of applicant or person authorised to sign on behalf of applicant

☒ I am making this application, or am authorised to sign on behalf of the applicant or applicant organisation.

☒ I have completed this application to the best of my ability and, as far as I am aware, the information I have provided in this application form is correct.

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Appendices and referenced material (if any) and glossary (if required)

References

Briese, D.T., Walker, A. (2002) A new perspective on the selection of test plants for evaluating the host-specificity of weed biological control agents: the case of Deuterocampta quadrijuga, a potential control agent of Heliotropium amplexicaule. Biological Control 25: 273−287.

Buhr, H. (1964) Bestimmungstabellen der Gallen (Zoo- und Phytocecidien) an Pflanzen Mittel- und Nordeuropas. Band I. G. Fischer Verlag, Jena, 761p.

Cai, Y.-F., Li, S.-W., Liu, Y., Quan, S., Chen, M., Xie, Y.-F., Jiang, H.-Z., Wei, E.-Z., Wang, L., Zhang, R., Huang, C.-L., He, X.-H., Jiang, M.-F. (2009) Molecular phylogeny of Ranunculaceae based on internal transcribed spacer sequences. African Journal of Biotechnology 8: 5215−5224.

Craig, T.P., Itami, J.K., Horner, J.D., Abrahamson W.G. (1994) Host shifts and speciation in gall- forming insects. In: Price, P.W., Mattson, W.J., Baranchikov, Y.N. (Eds). The ecology and evolution of gall-forming insects. General Technical Report NC-174, USDA Forest Service, pp. 194–207.

Dong, Y., Sun, Y-M., Zue, X-F (2016) Two new eriophyid mite species associated with Clematis terniflora var. mandshurica in China (Acari, Eriophyidae). ZooKeys 621: 1−14.

Fowler, S.V., Paynter, Q., Dodd, S. & Groenteman, R. (2012) How can ecologists help practitioners minimize non-target effects in weed biocontrol? Journal of Applied Biology 49: 307–310.

Frago, E. (2016) Interactions between parasitoids and higher order natural enemies: intraguild predation and hyperparasitoids. Current Opinion in Insect Science 14: 81−86.

Gourlay, A.H., Wittenberg, R., Hill, R.L., Spiers, A.G., Fowler, S.V. (2000) The biological control programme against Clematis vitalba in New Zealand. In: Spencer, N.R. (Ed.). Proceedings of the X International Symposium on Biological Control of Weeds, 4–14 July 1999, Montana State University, Bozeman, Montana, USA, pp. 709–718.

Greer, G., Sheppard, R.L. (1990) An economic evaluation of the benefits of research into the biological control of Clematis vitalba L. Research Report No. 203, Agribusiness and Economics Research Unit, Lincoln University, 45p + appendices.

Groppe, K. (1991) Literature review and preliminary survey for biotic agents associated with old man’s beard, Clematis vitalba L. Unpublished Progress Report, International Institute of Biological Control, Delemont, Switzerland, 39p.

Hong, X., Dong, H., Fu, Y., Cheng, L., Oldfield, G.N. (2001) Relationships between eriophyid mites and the host plants, with a case review of Eriophyoidea fauna of China. Systematic and Applied Acarology 6: 119-136.

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ISSG (Invasive Species Specialist Group). Clematis vitalba. http://issg.org/database/species/ecology.asp?si=157&fr=1&sts=&lang=EN (consulted May 2017).

Kaser, J.M., Ode, P.J. (2016) Hidden risks and benefits of natural enemy-mediated indirect effects. Current Opinion in Insect Science 14: 105−111.

Manaaki Whenua – Landcare Research (2018a) Host range testing of Aceria vitalbae. www.landcareresearch.co.nz/__data/assets/pdf_file/0005/139667/host-range-tests-aceria- vitalbae-for-clematis-vitalba.pdf

Manaaki Whenua – Landcare Research (2018b) Possible risks, costs and benefits of OMB control. http://www.landcareresearch.co.nz/__data/assets/pdf_file/0004/139666/potential-effects-to-be- addressed-aceria-vitalbae.pdf

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