EPA report

Import and release of pygmaeus (Rambur) March 2014

Advice to the Decision Making Committee on application APP201254: – To import and release as biocontrol agents for (Trialeurodes vaporariorum), under section 34 of the Hazardous Substances and New Organisms Act 1996

www.epa.govt.nz 2

Application for approval to import and release Macrolophus pygmaeus (APP201254)

Executive Summary and Recommendation

In November 2013, Tomatoes New Zealand made an application to the Environmental Protection Authority (EPA) seeking to import and release Macrolophus pygmaeus for use as an augmentative biocontrol agent to control in glasshouses. Their application stems from the desire to improve the competitiveness of the New Zealand tomato industry. The applicant asserts the key to improving competitiveness is the use of Integrated Pest Management (IPM) to manage pests in commercial glasshouses. Not only does this approach offer cost savings, it can reduce the use of harmful chemical inputs; improving people’s health, lowering environmental impacts and increasing the export potential of the product. We consider that IPM can, in the right circumstances, provide a win-win solution to both consumers and producers and we applaud this focus by the industry.

Integrated Pest Management by original definition is the integration of biocontrol with chemical applications, so that the latter have least impact on natural enemies. Thus a significant aspect of this approach is the use of natural enemies to control pests. This use of natural enemies has a long history both overseas and in New Zealand. To this effect the tomato industry is looking to introduce a new biological control agent (BCA), Macrolophus pygmaeus, a natural predator of the greenhouse whitefly (Trialeurodes vaporariorum). We recognise the need for additional pest control measures in New Zealand to provide for a rounded management programme, and we understand that Macrolophus pygmaeus is a candidate suitable for investigation. It is widely used in Europe and is potentially more effective at lower temperatures than agents currently available in New Zealand.

We have conducted a risk assessment under clause 27(1) of the Hazardous Substances and New Organisms (Methodology) Order 1998 (the Methodology)1, and weighed all the risks, costs and benefits associated with this application. Our risk assessment suggests that the applicant underestimated the risks, and may also be underestimating the benefit of releasing Macrolophus pygmaeus. The environmental risk of the release is New Zealand wide in scale and is irreversible. On the other hand, the applicant has not demonstrated the human health benefits to glass house workers, and the ongoing economic contribution of the tomato industry to the New Zealand economy.

Despite this it is worth noting the important social aspects of this application. The tomato industry, and in fact the wider horticultural sector, clearly needs and wants to increase its adoption of IPM, and we agree that new BCAs can play a valuable role in this. Furthermore, there is ongoing environmental damage occurring in New Zealand as a result of habitat modification from urban sprawl, dairying, increased infrastructure, indiscriminate agrichemical use, ongoing incursions, damage by existing vertebrate pests, and exploitation of our natural resources through fishing and mining for example. The Decision Making

1 Clause 26 of the Methodology states: Taking into account the measures available (if any) for risk management. The Authority may approve an application where a substance or organism poses negligible risks to the environment and human health and safety if it is evident that the benefits associated with that substance or organism outweigh the costs. Clause 27 states: (1) where clause 26 does not apply, the Authority must take into account the extent to which the risks and any costs associated with that substance or organism may be outweighed by the benefits.

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

Committee needs to be cognisant of these facts, and to take into account whether introducing Macrolophus pygmaeus presents risks and benefits over and above those already occurring in the country.

It is our recommendation that Macrolophus pygmaeus meets the Minimum Standards of the Hazardous Substances and New Organisms (HSNO) Act and therefore the crux of this decision is the weighting of benefits against environmental risk. Given the level of information we have available, our recommendation to the HSNO Decision Making Committee is to decline this application. While we do not consider that the risks pose significant harm to people, the environment or the economy, we do not consider that the applicant has made a strong case for the long term benefits to be realised. If anyone has more information that can clarify these benefits we encourage them to come forward at the hearing.

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

Table of Contents

1 The application process ...... 6 Purpose of this document ...... 6 The application ...... 6 Submissions ...... 6 Background ...... 7 New Zealand Biological Control Industry ...... 7 Industry pressure and ongoing need for Integrated Pest Management ...... 8 Glasshouse pests ...... 10

2 The organism proposed for release ...... 10

3 Risk and benefit assessment ...... 11 Minimum standards ...... 12 CLIMEX Modelling ...... 12 Habitat modelling ...... 14 Propagule pressure ...... 14 Dispersal ...... 15 Photoperiod ...... 16 Establishment potential ...... 17 Host range ...... 17 Plant host preferences ...... 21 Conclusion on the minimum standards ...... 22 The ability to establish an undesirable self-sustaining population and the ease of eradication . 23 Effects of any inseparable organism ...... 23 Adverse effects ...... 23 Adverse effects on fauna ...... 24 Adverse effects on flora ...... 25 Other adverse effects ...... 26 Precautionary approach ...... 27 Conclusion on adverse effects ...... 27 Positive effects ...... 27 Human Health ...... 27 Economic ...... 29 Conclusion on positive effects ...... 31 The Effects on the Relationship of Māori to the Environment ...... 31 Consultation ...... 31 Submissions ...... 32

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

Ngā Kaihautū Tikanga Taiao ...... 32 Impact on the Principles of the Treaty of Waitangi (Te Tiriti o Waitangi) ...... 33 Conclusion on Effects on the Relationship of Māori to the Environment ...... 34

4 Weighing of adverse and positive effects ...... 34

5 Recommendation ...... 37 Appendix 1A. Professor Jeff Bale CV...... 38 Appendix 1B. Comments provided by Professor Jeff Bale ...... 41 Appendix 2 Summary of Submitters ...... 49 Appendix 3 Comments from DOC ...... 54 References ...... 64

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

1 The application process

Purpose of this document

1.1 This document has been prepared by staff at the Environmental Protection Authority (EPA); Asela Atapattu (Manager, New Organisms), Kate Bromfield (Senior Advisor, New Organisms), and Manu Graham (Senior Advisor, Māori Policy and Operations), to advise the Hazardous Substances and New Organisms (HSNO) Decision Making Committee on the results of our risk assessment of an application to import and release Macrolophus pygmaeus as a biocontrol agent for whitefly in tomato glasshouses. The document discusses information provided in the application and other readily available sources.

1.2 This document has been reviewed by Professor Jeff Bale2 from Birmingham University, who specialises in the thermal tolerances of and the risk assessment of non-native biocontrol agents, and has worked extensively with Macrolophus spp. His comments are appended to this document in Appendix 1B. In addition, select New Zealand scientists3 reviewed this document as members of the EPA Insect Advisory Committee, to check for factual accuracy. The views expressed in this document, and the recommendations made by EPA staff, do not necessarily reflect the views of the independent experts who contributed to the review.

The application

1.3 The application to import and release Macrolophus pygmaeus was formally received by the EPA on 20 November 2013 under section 34 of the HSNO Act (the Act).

1.4 The goal of the application is to release M. pygmaeus as a natural predator to control greenhouse whitefly. Macrolophus pygmaeus is seen as an additional tool to be used in Integrated Pest Management (IPM) programmes in commercial greenhouses, potentially reducing reliance on chemical sprays and improving compliance with export and market access requirements.

Submissions

1.5 The application was publicly notified as required by section 53(1)(b) of the Act. The 30 working day notification period began on 29 November 2013 and closed on 7 February 2014.

1.6 Submitters were asked to provide information, make comments and raise issues, particularly with regard to the adverse and positive effects of the application.

2 A copy of his CV is provided in Appendix 1A. 3 D. Teulon (Chair), B. Barrat, T. Withers, S. Worner, J. Beggs, R. Hill, C. Green and J. Charles.

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

Submissions received through public notice

1.7 Thirty-four submissions were received during the submission period in response to public notification of the application. Twenty-three submissions were received in support; nine opposed, and two neither supported nor opposed, but expressed their concern over aspects of the application. The submissions are summarised in Appendix 2.

1.8 One late submission was received on 13 February 2014, from Mr Won Ha Park. Under s59(3)(a)(i) of the Act the statutory time frame in which to receive submissions was waived by the Chair of the HSNO Decision Making Committee so that this submission could be considered by the Committee. This submission is also included in Appendix 2.

Submissions from MPI and DOC

1.9 As required by the Act and the Hazardous Substances and New Organisms (Methodology) Order 1998 (the Methodology), the Ministry for Primary Industries (MPI) and the Department of Conservation (DOC) were advised of the application and provided with the opportunity to comment. MPI did not comment on the application, but provided advice when requested under s58(1)(a) of the Act. Their comments are incorporated into the text of this document. We gave particular regard to the comments provided by DOC, and these are provided in full in Appendix 3.

Background

New Zealand Biological Control Industry

1.10 New Zealand is well recognised for its stringent biosecurity provisions and strict rules around the importation of new organisms (Hunt et al. 2008). This approach was legislated for in 1996 with the promulgation of the HSNO Act, although this is not what New Zealand is internationally applauded for so much as a thorough, consultative, fair, public process which is time-bound. The biological control industry in New Zealand functions effectively within these legislative bounds (Hill et al. 2011).

1.11 However, we should highlight significant differences with respect to this application. Although there is a call for additional biological control agents from within the tomato industry, the organism in question is a zoo-phytophagous predator4 (Alomar et al. 2002), and is unlike the biological control agents historically approved by the EPA. Unlike previous applications, no active host range test trials have been undertaken by the applicant, there have been few intentional releases internationally, and some countries have opted to look for alternative agents on the grounds of biosafety risks.

4 The term refers to the fact this type of organism can survive on a diet of both plants and . In fact, M. pygmaeus is considered to be phytophagous (lives on plants) in the early stages of its life or in the absence of prey (Battaglia et al. 2013).

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

1.12 We acknowledge the importance of this application for industry. The use of Macrolophus has long been considered as an option for pest control, and industry documents from 2007 show the first signs of focused analysis. This was followed up in 2008 with an EPA approval to conduct basic research in containment on 10 , including Macrolophus, for the purpose of host specificity tests and evaluation as biological control agents for the greenhouse industry, although we are not aware of whether any progress has been made with this approval.

Industry pressure and ongoing need for Integrated Pest Management

1.13 The New Zealand Tomato industry produces approximately $110 million per annum of crop, of which approximately $10 million is exported (Tomatoes New Zealand 2014). Despite the potential for New Zealand to grow its net exports, there is stiff international competition and a market that is increasingly focused on capital-intensive production facilities and simultaneous potential price declines (for example: Cook & Calvin 2005; Martin-Rodriguez & Caceres-Hernandez 2013).

1.14 These pressures create an ongoing need for industry to invest in enhancing productivity. The applicant mentions recent changes in the New Zealand industry that have, for example, included upgrading glasshouses and moving to the use of soilless media. The industry continues to evolve and there is an ongoing trend in the reduction of pesticides. This is a result of both regulatory changes such as increasing restrictions on the use of chemicals such as organophosphates (EPA 2013), social pressure, the potential for increasing levels of chemical resistance in major pests (Martin et al. 2005), and catering to a demand from overseas markets for produce that has been grown with reduced chemicals. Studies from the late 1980s onwards show public awareness of the human health concerns from chemical residues, and demonstrate a willingness to pay up to 10% more for chemical free tomatoes (Weaver et al. 1992). Awareness and concern has only intensified in recent years, and regulatory changes reflect this. For example, tightening of European rules around agrichemicals could potentially remove a number of important crop protection

Figure 1 Principles of Integrated Pest Management products from the market (Hillocks 2012; (Reproduced from the U.S. Department of Agriculture) Hillocks & Cooper 2012).

1.15 Growers overseas have an array of naturally-occurring natural enemies that they can use to combat pests, many of which are not available in New Zealand. One reason for the available ‘array’ overseas is that most of them are native in those countries and/or that the countries do not regulate the

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

movement of insects between them. Consequently many countries have been able to run very successful IPM programmes (see Figure 1), and over 165 pest and weed species have been brought under permanent or temporary control through the use of biological control (Cock et al. 2009). Ongoing research suggests that well run IPM programs have multiple benefits. One extensive study of 62 projects in 26 countries found that 60% of the projects resulted in lower pesticide use and increased yields (Pretty 2008). An IPM approach emphasises the management of pests using the most economical means while reducing the hazard to people, property and the environment. In particular, IPM involves the judicious use of chemical pesticides, improving worker health and lowering the level of pesticide residues on crops.

1.16 The New Zealand tomato greenhouse industry professes to manage pests using an IPM approach. For example the greenhouse whitefly (Trialeurodes vaporariorum), the most common pest on greenhouse tomato crops, is managed using a combination of soft chemistry5, insect pathogens such as fungi, non-selective chemicals6, and the biological control agent Encarsia formosa. Unfortunately, New Zealand has had less success at controlling greenhouse whitefly than other countries as E. formosa, a relative mainstay of IPM biocontrol programs overseas, has not been as effective here. This may be because it does not perform well in low temperatures, is sensitive to changes in daylight (Zilahi-balogh et al. 2006), and does not attack all life-stages of whitefly (Bioforce 2014). Nicholas Martin’s submission on this application suggests that this weakness may also come from the “timing of crop planting and methods of transition from old to new crop [which] meant that most crops went into the winter with too many whitefly and the parasitoid was unable to control the whitefly in winter and spring.”

1.17 We are also aware that some growers, who grow under plastic rather than glass, believe that E. formosa is not effective under the resulting ultra-violet bandwidth (A. Ivicevich pers. comm. 2014).

1.18 Tomatoes New Zealand has identified M. pygmaeus as a potential release candidate for biocontrol of greenhouse whitefly that they consider will add another tool to their IPM toolbox. Their primary reasons for this choice are its:  Efficacy as a whitefly predator;  Ability to consume all stages of whitefly;  Ability to operate at lower temperatures than E. formosa; and  Proven efficacy at controlling pests on tomatoes.

5 Oils (e.g. Neem) and soap sprays. 6 Pesticides that can kill any pest are called broad-spectrum or nonselective pesticides.

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

1.19 Tomatoes New Zealand contends that the introduction of this organism will benefit both growers and the wider community by enhancing IPM in New Zealand. They also consider that this would increase the ability of tomato growers to compete with overseas producers.

Glasshouse pests

1.20 There are numerous pests of glasshouse crops, including thrips, psyllids, and (Pedley 2010). One of the most economically damaging of these is the greenhouse whitefly (Trialeurodes vaporariorum) which is the main pest species of greenhouse and outdoor tomato crops (Martin et al. 2005). The applicant states that greenhouse whitefly causes damage to tomato plants in a variety of ways. Both the juvenile and adult stages cause damage when they pierce the plants in order to suck plant juices. This direct feeding takes energy away from plant growth, and can also weaken the plant or introduce and vector pathogens. Heavy feeding by whitefly can kill a plant. Moreover, the sugary secretions of a feeding whitefly can encourage fungi such as sooty moulds to grow, which can damage the plant and make much of the produce unsellable.

1.21 Greenhouse whitefly is capable of reproducing quickly, has the ability to disperse easily and is capable of feeding on a wide range of plants, including commercial crops such as tomato, capsicum, eggplant, cucumber, gerbera, sweet pepper, pumpkins, beans and tamarillo (Smith 2009).

2 The organism proposed for release

2.1 Macrolophus pygmaeus Rambur

Class: Insecta

Order:

Family:

Tribe:

Genus: Macrolophus

Species: pygmaeus

2.2 The applicant noted taxonomic uncertainty surrounding this organism although they also noted new technology has helped resolve this: “Recent use of molecular tools to determine species identity has concluded that the commercial BCA labelled as M. caliginosus was in fact M. pygmaeus (Martinez- Cascales et al. 2006a, 2006b)”. They mentioned that much of the literature from which they draw their assessment uses the term M. caliginosus to describe M. pygmaeus.

2.3 We consider that methods are now available for adequately identifying the organism, including molecular methods as described in Evangelou et al. (2013). We also note that in early literature the

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

use of M. caliginosus and M. pygmaeus can cause confusion and care needs to be taken when utilising such references.

2.4 The applicant has also provided us with information about other countries where M. pygmaeus is used, stating in the application that there is “Widespread commercial use overseas for example: Koppert (Mirical), Syngenta Bioline in the USA, Canada, UK and Netherlands (Macroline p), Biobest.com (Macrolophus System)”.

2.5 Macrolophus pygmaeus is widely used in Europe and some unspecified countries in Africa (van Lenteren 2012) but we found no evidence of it being used in the USA or Canada. In fact, we have found evidence to the contrary. For example, Gillespie et al. (2007) stated that “The success of M. caliginosus in Europe prompted greenhouse tomato growers in North America, particularly in British Columbia, Canada, to lobby for its importation. Our consultation with Canadian regulatory authorities confirmed that permits for importation of M. caliginosus were unlikely to be issued in either Canada or the USA. Therefore, a project to develop a native natural-enemy species, with the characteristics of M. caliginosus, was initiated”. This is also mentioned in literature cited in the application; Castañé et al. (2011) noted “The use of this predator [ hesperus] began when the Canadian greenhouse industry sought to apply similar biocontrol alternatives to those developed in Europe with M. pygmaeus, a Palaearctic species that could not be imported [emphasis added].”

2.6 The lack of use outside its native range makes it difficult to predict the results of releasing M. pygmaeus. We draw attention to this problem later in our assessment.

3 Risk and benefit assessment

3.1 EPA staff have conducted a risk benefit assessment for the import and release of M. pygmaeus. This includes assessing potential risks and benefits to the environment, human health and safety, Māori culture and spiritual values, society and community, and the market economy.

3.2 The applicant has suggested that this organism could provide significant benefits to the industry with low environmental risk. In assessing the application we have determined that there are gaps in the information available on the risks, but we also consider that some of the information provided in the application is flawed. For example, some references are incorrectly cited, and the models presented appear to have been misinterpreted. However, using readily available literature, and information obtained during the public submissions period, we have been able to undertake a complete risk assessment on the risks costs and benefits associated with releasing M. pygmaeus.

3.3 We are not using the qualitative descriptors shown in the application (see page 16, section 6.2, Table 1 of the application) because the in-built exchange rates between risks and benefits within that

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

framework were not constructed with this type of application in mind. Such descriptors over simplify the trade-off between environmental risks and economic benefits, for example, and we do not consider that they play an appropriate role in evaluating the risks, costs and benefits of the application.

Minimum standards

3.4 Prior to approving any new organism for release, the EPA is required to ensure that the organism meets the minimum standards set out in section 36 of Act.

3.5 Our consideration of these significant effects is limited in this section of the Act “to native species within their natural habitat”, and to the “deterioration of natural habitats”. We do however consider “all the effects of the organism” in s38(a)(ii) of the Act, and these will be discussed later in this document.

Section 36 (a): whether Macrolophus pygmaeus is likely to cause any significant displacement of any native species within its natural habitat.

3.6 The applicant has provided evidence from CLIMEX modelling and habitat matching which show the potential for M. pygmaeus to establish in parts of New Zealand. We support the use of multiple models by the applicant to model risk; however, we question their interpretation of the modelling results. Professor Bale noted that “Whilst the accuracy of this modelling technique and its interpretation can be questioned, it seems to beg a wider question: is any level or locality of establishment of a non-native species acceptable?” We consider that section 36 of the Act does not ask us to consider “any displacement of any native species; any deterioration of natural habitats; any adverse effects on human health; or any adverse effect to New Zealand’s inherent genetic diversity”, but rather asks us to consider what level of effect we deem “significant”.

CLIMEX Modelling

3.7 The CLIMEX mode presented in Appendix 9.5 of the application incorporates physiological data and models the potential distribution of M. pygmaeus in New Zealand. It shows that M. pygmaeus could survive some of the year in restricted areas of the North Island, but these would be limited to warmer areas north of Auckland and on the eastern coast. We have some misgivings with regards to the accuracy of this model. For example, all sites in the UK are recorded as unsuitable, yet we know that M. pygmaeus is overwintering (Hart et al 2002), and spreading there. Furthermore, sites in Southern France where the current commercial strain of M. pygmaeus was collected (Sanchez et al. 2012), are areas that register only as ‘marginal’ or ‘suitable’, despite the fact that we know M. pygmaeus does well outdoors in this area (K. Alcock, pers.comm. 2013). Certainly if we were to interpret areas considered ‘suitable’ as potential locations for establishment, we expect that the picture would change dramatically from the northern and eastern North Island to all of the North Island except for the colder central regions.

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

3.8 Furthermore, the application creates confusion about the locality records used to inform the model parameters. Locality records were taken from published papers and online databases, and then any records pertaining to covered crops or glasshouses were removed. A more thorough analysis of these locality records would have given us more confidence in their model. However, we understand that this is extremely hard as it is difficult to find an accurate description of the range of M. pygmaeus. For historical background, Sanchez et al. (2012), suggested that populations of M. pygmaeus retreated to the Iberian, Italian and Balkan peninsulas and possibly southern France during glaciation events in Europe, then spread from there during warmer interglacial periods. This is demonstrated in the United Kingdom: based on genetic analysis of populations distant from any releases, Sanchez et al. (2012), considered the UK population to be native. Other material also indicates that M. pygmaeus is part of the UK fauna and widespread but not common in the environment (HDC 2013). To add to the confusion, the organism released in the UK as M. caliginous in 1995 is now likely identified as M. pygmaeus (HDC 2013), leaving us with the puzzle of why this introduced population behaves differently from the local population. We consider that these populations may be different ecotypes although this remains unstudied. With this in mind, we note that recent publications sample M. pygmaeus from locations that the applicant has noted, as well as Turkey, the UK, and France (Sanchez et al. 2012), and further publications may provide additional field records (e.g. Machtelinckx et al., 2012)7.

3.9 Although some of these records likely refer to glasshouse use (some records we can infer from the GPS location as being next to a plant nursery or glasshouse), others we are less sure of. In light of the taxonomic uncertainty surrounding M. pygmaeus and the critical importance of accurate modelling we reiterate that we would have liked to see the applicant provide a careful analysis of each available publication.

3.10 In addition, we consider that a degree of error has crept into the CLIMEX interpretation due to confusion between Macrolophus melanotoma (= Macrolohus caliginosus) and Macrolophus pygmaeus. The applicant mentions that “In any case the response to climatic variables may only differ slightly between M. pygmaeus and M. melanotoma as they are largely sympatric”. Although there is some evidence to suggest an overlap in parts of their distribution, we note that there is also information that suggests otherwise. For example, Perdikis et al. (2000) noted that

7 In addition, review papers record its distribution as including Algeria (Zappalà et al. 2013), and large accessible databases such as the Global Biodiversity Information Facility, records 172 collections from Germany, Sweden, the UK, Finland, Poland, Luxembourg, Austria, Norway and Ireland (GBIF 2013). Likewise, the European Fauna Database, records M. pygmaeus from a variety of areas including Albania, Austria, Azores, Belarus, Belgium, Bosnia and Herzegovina, Britain, Bulgaria, Croatia, Czech Republic, Danish mainland, European Turkey, Finland, French mainland, Germany, Greek mainland, Hungary, Ireland, Italian mainland, Luxembourg, Macedonia, Madeira, Malta, Moldova, Republic of, Norwegian mainland, Poland, Portuguese mainland, Romania, Russia North, Russia South, Slovakia, Slovenia, Spanish mainland, Sweden, Switzerland, The Netherlands and the Ukraine (Fauna Europaea 2013).

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

“M. caliginosus mortality recorded at 30°C was much higher than that for M. pygmaeus (46.43 and 20%, respectively), suggesting that the latter species can better tolerate higher temperatures.”

3.11 We understand that accurate record identification is time consuming and difficult, but in order for a model to be useful in a risk assessment process, it needs to be researched thoroughly and accurately. Without this information caution must be used when interpreting the areas that the CLIMEX model has identified as optimal and suitable.

Habitat modelling

3.12 The applicant has provided an alternative modelling approach (see Appendix 9.6 of the application), to predict the potential establishment of M. pygmaeus. The method matches known overseas geographic records to New Zealand conditions. The application states that “the consensus multi-model indicated that only a small area of Kaitaia in Northland has suitable climate for M. pygmaeus.”

3.13 We consider that the Maxent predictions in particular are fundamentally flawed. Only 23 field records are available, falling below the 30 that the report’s author recommends for accurate predictions and the author (not the applicant) noted that “As the collection data for each of the three BCAs were limited…the models may be inaccurate and caution is advised in interpreting the results”. The authors then go on to note that “… in this case CLIMEX results may be more reliable than Multi Model and Maxent model results” (see Appendix 9.6, page ii of the application).

3.14 We are concerned about the accuracy of both models relied on in the application, and by the applicant’s interpretation of the information the modelling provided. We consider that the models indicate the potential for M. pygmaeus to establish across a much wider geographical range than provided for by the applicant.

Propagule pressure

3.15 Organisms that are released repeatedly and in high numbers have a greater chance of establishing (Lockwood et al. 2005). Although much of this research is focused on vertebrate populations, evidence suggests that invertebrates often require few individuals to be released in order for a population to establish. For example, work conducted in New Zealand using gorse thrips found releases of 10 insects were unlikely to establish, but releases of 30 insects held a much greater chance of being located 1 year after they were released (Memmott et al. 1998). Further work by the same primary author, this time using a pysllid weed biocontrol, found 20% of releases of two adults, and 40% of releases of four adults successfully established (Memmott et al. 2005). Interestingly, the latter study found that populations declined in the first year, but after this they increased and if they were able to survive this first critical year, they had on average a 96% chance of surviving thereafter, providing that the site remained secure (Memmott et al. 2005).

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

3.16 We have not found any specific information on the number of M. pygmaeus individuals required to enable the formation of a population.

Dispersal

3.17 The literature on dispersal makes it difficult to provide an unequivocal answer for M. pygmaeus with respect to the rate at which it could spread into the environment. The species does not develop large populations rapidly, and dispersal appears to be influenced by the quality and distribution of surrounding food sources (Put et al. 2012). While little is known about the key environmental triggers that cause M. pygmaeus to disperse (Alomar et al. 2002), there are indications that it disperses readily into areas with abundant, complex vegetation, specifically cropland (Alomar et al. 2002; Gabarra et al. 2004), but that greenhouses may limit the immigration of mirids such as Macrolophus (Gabarra et al. 2004). Little research was found investigating the specific dispersal ability of M. pygmaeus. One study reported that M. pygmaeus was able to colonise the study site from the surrounding vegetation at distances greater than 75m (Alomar et al. 2002).

3.18 This information needs to be tempered with a number of other important elements. One of these is the sensitivity of M. pygmaeus to insecticides, a variety of which have been tested (Rasdi et al. 2012; Arnó & Gabarra 2011; Tedeschi & Tirry 2002; Nannini et al. 2012; Martinou et al. 2014). Furthermore, crop de-leafing and pruning has also been found to have a negative impact on the dispersal potential of Macrolophus (Alomar et al. 2006; Bonato & Ridray 2007).

3.19 In principal we consider that for M. pygmaeus to enter natural habitats, it must pass through highly modified (local) environments (Figure 2), and that there is reason to believe that M. pygmaeus ‘escapees’ will struggle in areas where insecticides are regularly applied and disturbance is regular. However, once widely used, there would be a complete range of surrounding vegetation in glasshouse production areas, and even potentially home gardens, which may be full of suitable prey items to support the dispersal of M. pygmaeus through these environments and into natural habitats.

3.20 We therefore consider that on the basis of probabilities, M. pygmaeus will reach areas of native habitat. It can survive on many plants (Table 1), and is able to utilise a wide variety of prey (Table 2). The primary pest to be controlled, the greenhouse whitefly, has a large host range and although we could not find information on its exact distribution we expect it to be present in many areas. Many other prey species are also widespread in the New Zealand environment. Furthermore, many of the plant species that M. pygmaeus is capable of utilising and reproducing on are also widespread. For example, there are at least two Solanum species that could be suitable hosts and that are recognised as weeds of pasture areas (Matthews 1984).

3.21 If M. pygmaeus were made available on the retail market to any glasshouses, including commercial and personal, then it will have ample opportunities to disperse. In addition, the large number of people

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

Figure 2 Distribution of effects, from individual through to regional. This figure also describes the passage of M. pygmaeus from the glasshouse, through modified cropland (local) and into natural habitats.

who regularly walk in and out of glasshouses should be considered as a further opportunity for M. pygmaeus to spread, along with tomato material and waste moved in and out of these facilities, and we are also mindful of long distance dispersal on the wind (for example: Ducheyne et al. 2007; Wiktelius 1981).

3.22 We do not consider that dispersal will be a limiting factor for the establishment of M. pygmaeus.

Photoperiod

3.23 In the application, information is provided on a study by Hamdan (2006), which looked at the development cycle of M. pygmaeus in relation to photoperiod. The applicant used this information to state “reducing day lengths from 16hr to 8hr or to continuous dark exposure had a significant effect on the development of Macrolophus embryos by causing embryo hatch rates to reduce under reduced daylight hours, or cease in the case of no light exposure”.

3.24 We consider that caution should be used when interpreting this information. The applicant ignores other relevant results from the study, including that the photoperiod had no effect on total offspring per female, nymphal mortality or adult longevity. The study also showed that nymphs feed more when under constant darkness (Hamdan 2006), a finding tentatively supported by other research (Perdikis et al. 1999).

3.25 Furthermore, we believe the logic the applicant has applied in this situation is tenuous and needs to be clarified. Failure of a percentage of eggs to develop does not prevent the formation of a self-sustaining

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population. Field trials in the UK show that mortality in the winter increases with time, but if able to access food, a significant proportion of both adults and nymphs can survive for well over 50 days (Hart et al. 2002). This would enable a population to survive a New Zealand winter and expand during warmer months even if no eggs were able to develop over the winter months.

Establishment potential

3.26 The application is predicated on the belief that self-sustaining populations will not establish. We disagree with this analysis and our view is that it is very possible that M. pygmaeus will establish a self-sustaining population. Many submitters, but DOC in particular, commented that “With the reliance on temperature we would have expected a discussion on the potential, if not actual, effects of climate change on distribution limits. However, there is no reference or discussion on this at all. Climate change, as a real phenomenon, is increasingly being accepted by the world’s scientific community. Its effect on New Zealand’s climate would, in all likelihood, lead to an increase in the potential distribution of M. pygmaeus beyond the areas indicated by the modelling in the application.”

3.27 We consider that M. pygmaeus is likely to establish in the foreseeable future, with or without climate change (unless of course the climate were to become significantly colder). We do not consider that additional analysis of the CLIMEX or habitat matching models to incorporate future climate scenarios would have changed our analysis.

Host range

3.28 In light of our assessment on establishment potential, it is important to assess the risk that M. pygmaeus will cause significant displacement of native species within their natural habitat. This is particularly important for M. pygmaeus which is zoophytophagous, meaning it is capable of feeding on both plant and material.

3.29 The applicant noted that M. pygmaeus consumes all stages of whitefly and also eats aphids, two- spotted mite, insect eggs, caterpillars, thrips and leaf miner larvae. The applicant then summarises what this may mean in a New Zealand context (Table 2. section 6.3.1 of the application).

3.30 We agree in broad terms with their summary. We have reviewed the literature on predatory behaviours drawing on laboratory studies, as well as the artificial diets that have been tested for rearing M. pygmaeus (Table 2). There are few, if any, real studies on the predatory behaviour of M. pygmaeus in the field. Therefore, while laboratory studies are known to modify behaviour compared to the way organisms behave in the environment, we have drawn on any results from laboratory studies we can find. To demonstrate the potential scale of this bias, Lucas et al. (2009), detected intra-guild predation between Dicyphus tamaninii and in artificial environments, but found no evidence of this in a more natural setting.

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3.31 Although M. pygmaeus is nominally referred to as a whitefly specialist, this assertion appears to be used regularly with little justification. For example one study showed that when the preference of Macrolophus was tested with two-by-two choice tests, Macrolophus preferred active prey over eggs but no other preferences were detected (Tedeschi et al. 1999)8. In an experiment using the greenhouse whitefly and two-spotted spider mite, the results indicated that Macrolophus preyed on each species in roughly equal proportions. However, once whitefly proportions rose above 70-80% its preference shifted towards whitefly (Enkegaard et al. 2001). Other studies have suggested that M. pygmaeus does have prey preferences; for example when provided with two species, it consistently predated Myzus persicae at a higher rate (Lykouressis et al. 2007). Likewise, Bonato et al. (2006) found that Macrolophus prefers greenhouse whitefly over , although once again this preference tended to disappear once the proportion of silverleaf whitefly exceeded >75- 80%. On the basis of these results it would appear that the prey items that M. pygmaeus will focus on is density dependent. Real world outcomes will be dependent on the density of prey in the environment, the life-stages present and the size of the prey. We note the importance of considering the population size of M. pygmaeus and its growth rate. Obviously larger populations that grow faster have the potential to consume more prey, although indications are that population increase is maximised in the presence of preferred prey (for example, Trottin-Caudal et al. 2012).

3.32 Based on this information, we conclude that native species would potentially form part of the diet of M. pygmaeus. With respect to significant displacement, we focus our attention on the area reportedly most suitable for M. pygmaeus; Northland. Northland is home to many endemic invertebrates (for example: Winterbourn 2009; Buckley & Bradler 2010), and has a large proportion of threatened and rare species (Lux et al. 2009), including invertebrates (McGuinness 2001). Unfortunately, many of our endemic invertebrates have not been described, let alone their distributions mapped (McGuinness 2001), so it remains difficult to determine exactly what level of impact M. pygmaeus might have, and on which species.

3.33 A recent threat classification of the family Aphididae provides us with an example of the threats faced by native invertebrates. Of the 11 taxa classified, three are considered nationally critical, the highest level of threat. The other taxa are generally ranked as data deficient (4) and nationally uncommon (3) (Stringer et al. 2012). Examples include Aphis nelsonensis which has been collected from only two sites and may now be considered extinct as it has not been found since 1995 (Teulon et al. 2013). Obviously any non-target effects on such a rare species could easily threaten their viability; however, this needs to be balanced with the likelihood that both species would actually come into spatial and

8 These reports were provided at an international conference and we were only able to access the abstract.

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temporal contact, given that M. pygmaeus feeding is density dependent, and rare species exist in lower densities.

3.34 Paradoxaphis plagianthi is an aphid listed as relict. It appears to be locally common in Christchurch city; however, its distribution has shrunk rapidly, and this is the reason for its relict classification (Stringer et al. 2014). This decline in population is the result of human activities such as the removal of significant trees. We consider that predation by M. pygmaeus is unlikely to have a greater impact on this species than habitat loss already in progress. We understand that to add yet another stress factor could tip the balance, and that to think further risk will not make any difference is dangerous, but we consider that a context for risks already present in New Zealand is an important factor in the evaluation of this organism.

3.35 We acknowledge that should M. pygmaeus encounter a rare or threatened population, some people will consider any effect significant, but it is not clear that M. pygmaeus would be the primary cause of any resultant displacement or population decline. Risks to our threatened invertebrates appear to be caused by predation and habitat modification, with the prime suspects being rodents, possums and pigs (McGuinness 2001). Although the predatory behaviour of M. pygmaeus could obviously be harmful to any threatened species we do not consider the significance of this threat to be as high as mammalian predation on plant host species (i.e. possum damage), and habitat modification. Further, we consider these pressures are occurring on native species despite management efforts to reduce them.

3.36 We note the usefulness of taking a severity approach in this instance due to the lack of specific information on M. pygmaeus. Table 3 shows a severity index (SI) developed by Lynch et al. (2001) that can guide the assessment of significance. It is based around the concept that a mortality level of at least 40% is necessary in order to lead to a population-level impact (Lynch et al. 2001) and although we admit to the crudity of this measure, it does provide perspective. For example, the authors categorised Microctonus aethiopoides, a parasitoid released in New Zealand, as severity level three after field studies by Barratt et al. (1997) recorded it parasitising seven genera in three tribes of two subfamilies. On the other end of the scale, Vespula wasps are one of the worst invertebrate pests in New Zealand, reach high densities, and feed aggressively on a variety of prey and food sources (in addition to being generalist predators they feed on plant sap). They have a profound impact on native species experimentally placed in their vicinity, with some having virtually no chance of survival (Beggs 2001). Such effects have likely led to invertebrate declines and at least local extinctions, and we consider this makes wasps a candidate for severity level seven and above.

3.37 We note that the polyphagous nature of M. pygmaeus and its ability to utilise a wide range of plant hosts, gives it many of the characteristics of a successful invader. Although we can see no mechanism

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

for M. pygmaeus to be as damaging as wasps, we predict that its predatory nature and wide host range is likely to make it more harmful than Microctonus aethiopoides. We have therefore assigned it a range of four to seven on the severity index, as this lies between the SI nominally assigned to Vespula and Microctonus aethiopoides.

3.38 DOC commented that “As well as direct predation to our endemic insect fauna there is the possibility of competitive displacement. This threat is particularly significant for host specific invertebrates such as the 3-4mm long mirid Pimeleocoris viridis. This endemic species is listed as Nationally Critical by Stringer et al., (2102b) and is found only on a single host plant species Pimelea villosa villosa which itself is listed as Declining (de Lange 2009) and is only known from a small area near Kaitaia (Stringer et al., 2012b). The application acknowledges that if M. pygmaeus is capable of establishing anywhere in New Zealand it would be in this area. This could thus pose an extreme risk to the survival of this endemic mirid”.

3.39 It is worth comparing the potential impacts of M. pygmaeus to the actual effects from a native (or naturalised) mirid, Ausejanus albisignatus (previously Sejanus albisignata/S. albisignatus). This mirid is also zoo-phytophageous (Wearing & Attfield 2002), is found on a huge range of native and introduced plants (Eyles & Schuh 2003), and may even cause crop damage (Wearing and Attfield 2002). Although we understand that any balance currently occurring in New Zealand’s natural habitats may be disrupted by the introduction of a new mirid, in the context of risk, the introduction of M. pygmaeus does not pose any new or greater risk to native species’ existing in these habitats.

3.40 We hesitate to ascribe an exact level of impact and have instead provided a range of effects for consideration. We consider that the overall risk is non-negligible, but the specific risk of significant displacement of native species in their natural habitats is unlikely.

Section 36 (b): whether Macrolophus pygmaeus is likely to cause any significant deterioration of natural habitats.

3.41 For the purposes of this section we believe it is worth clarifying what we mean by natural habitats. The Oxford dictionary defines natural as “1a existing in or caused by nature, not artificial. 1b uncultivated; wild”. We acknowledge that some people would incorporate any habitat with a large number of native species in their definition of natural habitat, and that habitat is inextricably linked to biodiversity. To define it otherwise would immediately discount the biodiversity values associated with disturbed habitats and the remnant flora and fauna that might occur there. It would discount things like bush remnants on farms, and native vegetation filled with weeds. We however, do not to refer to these (manmade or modified) areas. Instead we interpret natural habitats to include unmodified areas that have been principally set aside for the management of biodiversity outcomes.

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

3.42 The applicant has provided little information on whether M. pygmaeus is likely to cause significant damage to natural habitats and makes no real comment on the issue. Our assessment focuses on potential damage to natural habitats caused by damage to plant hosts.

Plant host preferences

3.43 Should environmental conditions be suitable for establishment of M. pygmaeus in New Zealand, it is important to know which host plants it may seek out and establish populations on. The application investigates this, but the analysis is not comprehensive. In the section on biological characteristics (Appendix 9.3 of the application), the applicant states that “Macrolophus pygmaeus …is mainly found on solanaceous plants, particularly tomato and tobacco, but can also inhabit other crops (Malais & Ravensberg, 2003)”. No further mention is made of these ‘other crops’ but they do mention that “Overseas data records a few main plant hosts within the Solanaceae, Lamiaceae, and Geraniaceae”. The applicant suggests that in these three potential families there are 197 species in New Zealand, of which 18 are native and 10 of these exhibit leaf morphologies that make them potential host plants.

3.44 When we analysed the readily available literature we found that M. pygmaeus has been recorded on or studied in the lab using up to 8 plant families (Table 1). It is important to note that nymphs of M. pygmaeus have been found to complete development on three of these families (Cucurbitaceae, Fabaceae, and Solanaceae) in the absence of prey. If we use the applicants approach and extrapolate the analysis of New Zealand species in the 8 plant families, the total is 1152 species of which 447 are native.

3.45 Dr. Steven Pawson submitted on behalf of the Entomological Society of New Zealand that “The applicant does not provide any empirical evidence to determine if native Solanaceae, Lamiaceae and Geranicaceae will be suitable host plants and what impact this may have on these plants and associated native invertebrates. Such fundamental host range testing should be conducted prior to a release”.

3.46 After considering the available information, we assume that M. pygmaeus is likely to be able to survive and complete its development on some native plant species. However, we consider it unlikely that the release of Macrolophus pygmaeus could cause significant plant damage to native species and therefore cause significant deterioration of native habitats. This specific risk is therefore negligible.

Section 36 (c): whether Macrolophus pygmaeus is likely to cause any significant adverse effects on human health and safety

3.47 We have not found any evidence to suggest that M. pygmaeus causes significant harm to people. It is widely used in European glasshouses at high densities. We would expect any human health impacts to be well recorded and the lack of these suggests it poses little risk.

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

3.48 We therefore consider that Macrolophus pygmaeus is not likely to cause significant adverse effects on human health and safety.

Section 36 (d): whether Macrolophus pygmaeus is likely to cause any significant adverse effect to New Zealand’s inherent genetic diversity

3.49 We acknowledge that the introduction of any new organism to New Zealand has the potential to cause harm to New Zealand’s genetic diversity. This effect could result from interbreeding between the introduced organisms and any closely related native organisms.

3.50 We were only able to find one record of cross-breeding attempts. In this study males and females of M. pygmaeus were allowed to cross with males and females of M. melanotoma. Results indicated the mating did occur, and eggs were oviposited, but none of these were viable (Perdikis et al. 2003). Given that viable offspring were unable to be produced in a close relative, it is unlikely that M. pygmaeus will cross-breed with any species present in New Zealand.

3.51 We also consider the possibility that the genetic diversity of New Zealand could be adversely affected if M. pygmaeus caused the extinction of any native species. We have discussed this eventuality in previous sections.

3.52 We therefore consider that Macrolophus pygmaeus is unlikely to cause any significant adverse effects to New Zealand’s inherent genetic diversity.

Section 36 (e): whether Macrolophus pygmaeus is likely to cause disease, be parasitic, or become a vector for human, animal, or plant disease.

3.53 We have not found any evidence or reports to suggest that M. pygmaeus transmits or vectors plant or animal diseases. It is worth noting that tomato potato psyllid vectors a new to science disease (Liberbacter), so there is a remote possibility that any new organism released into New Zealand could carry a disease that has yet to be described.

3.54 In light of the widespread use M. pygmaeus, and the probable immediate recognition of significant viral transmission, we consider that Macrolophus pygmaeus is not likely to cause disease, be parasitic, or become a vector for human, animal, or plant disease.

Conclusion on the minimum standards

3.55 We consider that Macrolophus pygmaeus is likely to cause displacement of native species in their natural habitats, cause deterioration of natural habitats, and have adverse effects on New Zealand’s inherent genetic diversity. However, we do consider that these effects are likely to be significant in the foreseeable future. We do not consider that Macrolophus pygmaeus is likely to have any significant adverse effects on human health and safety, nor is it likely to cause disease, be parasitic, or become a vector for human, animal, or plant disease.

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

3.56 Therefore, we consider that Macrolophus pygmaeus meets the minimum standards as stated in s36 of the Act.

The ability to establish an undesirable self-sustaining population and the ease of eradication

3.57 Based on the information assessed we consider that a self-sustaining population could form. However, we do not consider that any population formed would trigger the minimum standards and would therefore not be classified as undesirable. Given the effectiveness of particular insecticides, it may be possible to eradicate small and localised populations, but it would be difficult to eradicate widespread populations without significant non-target effects should the need arise.

Effects of any inseparable organism

3.58 It is a legislative requirement under section 38(a)(ii) that the Decision Making Committee consider the effects of any likely inseparable organisms. The applicant does not mention any, but we are aware of a number of endosymbionts associated with M. pygmaeus. These include Wolbachia pipientis, Rickettsia bellii and Rickettsia limoniae (Machtelinckx et al. 2012). These are particularly relevant when discussing the likelihood of establishment, as the removal of these endosymbionts increases the organisms tolerance to cooler temperatures (Maes et al. 2012). In addition, the presence of symbionts like Wolbachia can impact on the reproductive potential of the organism. In the case of M. pygmaeus evidence suggests that it induces abnormally severe cytoplasmic incompatibility, meaning that crosses between infected males and uninfected females almost always resulted in laid eggs failing to develop. It is therefore worth considering any fitness level effects of Wolbachia infection on the use of M. pygmaeus as a biological control agent (Machtelinckx et al. 2009).

Adverse effects

3.59 The applicant has identified potential adverse effects on the environment, on society and communities, and on the market economy, associated with the release of Macrolophus pygmaeus. They consider that the release of M. pygmaeus has the potential to;  Impact on native insect populations; and  Feed on plant tissue and damage crops.

3.60 We have also identified a number of potential adverse effects, via our public consultation process. These include;  Off-target effects on non-native but valued fauna; and  Adverse effects on crops.

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

Adverse effects on fauna

3.61 The applicant notes that M. pygmaeus was introduced into the UK in 1995 (Hatherly et al. 2005) and despite being subsequently detected outside of UK greenhouses no negative impacts have been documented (Castane et al. 2011; Hatherly et al. 2005; Hart et al. 2002). Unfortunately, although we consider it likely the applicant is correct in stating there are no recorded off-target effects; we do not consider that these references are correctly cited. Two of these papers make no mention of non-target effects and the third, Castane et al. (2011) is focused on plant host damage.

3.62 When assessing the risks to valued fauna we need to look at two important areas, (1) the localised effects of releasing large number of M. pygmaeus in inundative or augmentative releases and (2) large scale impacts from established populations. We also need to consider the mechanisms by which risks spread through environments and cause local to regional effects (Figure 2).

3.63 We have assessed the local impacts of M. pygmaeus in natural habitats above and found that while negative effects are likely; these are unlikely to trigger the minimum standards. It is also important to assess the possible negative effects on valued but non-native species, and native biodiversity in modified environments. We note that these modified environments may contain high levels of biodiversity, with for example a high proportion of New Zealand native aphids found in these areas (Teulon et al. 2013). We know from work by Lynch et al. (2001) that inundative control agents, often generalists that unable to establish, can still cause population level impacts, with an estimated 49% of non-target species suffering ‘quite serious local population effects’. However, we also know that Bale (2011) reported no significant off-target effects from the M. pygmaeus in the UK, despite its being known to be established there (although as above, we note it also occurs there naturally and as such presents a slightly different scenario).

3.64 Nicholas Martin submitted that “The authors of this report seem to be unaware that in the modified environment, there are several native insects that are predators of both native fauna and pests in crops. Bearing in mind the mirids preference for small prey including eggs, the eggs and larvae of these native predators would be vulnerable to being preyed upon by the mirid. I understand that some of these native predators such as lacewings (Neuroptera) and hover flies (Diptera: Syrphidae) are important biological control agents in crops such as potatoes”. He also expressed concern that “As the application states, it [M. pygmaeus] is known to feed on whitefly, spider mites (Acari: Tetranychidae), aphids, insect eggs, caterpillars, thrips (Thysanoptera) and leafminer larvae (most likely dipteran pests of greenhouse tomatoes), but its host range may be greater as it takes careful and deliberate observations to define a predators true host range. It is therefore likely to feed on and endanger  native species in these taxa and  feed on biological control agents of weeds, notably Gargaphia decoris Drake, 1931 (Hemiptera: Tingidae) released for the biological control of Solanum mauritianum.”

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

3.65 Mike Sim submitted on behalf of Biobees Ltd. that “currently there are no effective biocontrol agents for [TPP]…and this gap in pest control often severely impacts upon the biological control of other pests, particularly whiteflies, as the chemicals used to keep the TPP under control are toxic to the beneficial insects being used…Observation by Peter Workman at Plant and Food Research…prior to the realisation that it had been imported illegally, showed that it would eat large numbers of TPP eggs and early instar nymphs…”.

3.66 We consider that there are non-negligible risks to valuable insects that are being used as part of current biocontrol programmes.

Adverse effects on flora

3.67 As mentioned M. pygmaeus regularly feeds on plants. Damage has been recorded on crops such as tomatoes and is generally associated with extremely high densities of the predator. Macrolophus pygmaeus feeds on the phloem and xylem from plants in both the absence and presence of prey (Faten Hamdi et al. 2013), and in the one study, where this was quantified using DNA techniques, approximately 30% of individuals had fed on tomatoes recently (Pumariño et al. 2011). However, it is extremely rare for significant plant damage to occur and this appears to happen only under extremely high abundances of the organism. For example, plant damage to tomatoes is described under laboratory conditions, but few field studies report damage (Lucas & Alomar 2002; Castañé et al. 2011). There have been a small number of real world incidents reported; Sampson and Jacobson (1999 cited in Castañé et al. 2011), reported a UK field study describing distorted leaf growth, necrotic spots on leaves, scars on fruit and fruit drop. Furthermore, a report by the UK Agriculture and Horticulture Development Board noted that upon release in the UK it was soon apparent that the predators were feeding on tomato plants when prey was limited (HDC 2013).

3.68 Therefore we have not identified any significant risk to native plant species, but we note that reports of damage to tomatoes could be a problem. Although use of M. pygmaeus in mainland Europe has generally been considered safe (Castañé et al. 2011), there have been reports of crop damage in the UK. Macrolophus pygmaeus reportedly became one of the most important pests of organic tomatoes in the UK, causing losses estimated at £72,000/ha per season, and it was not until numbers were controlled by spraying with natural pyrethrums that this damage was controllable (HDC 2013).

3.69 Without seeing the sector’s IPM manuals we are unable to assess the relative risk of crop damage. We assume that the industry is aware of these facts and still considers that the benefits outweigh any such costs. This assumption is based on the sector having found value in submitting this application to the EPA.

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

Other adverse effects

3.70 Macrolophus pygmaeus is not used widely in IPM programmes except in Europe, and the possibility that M. pygmaeus becomes a quarantine pest on exported produce needs to be considered. This is difficult without knowing the exact IPM approach the industry will take. We do however note that Macrolophus is known to oviposit on stems, and more rarely on tomato leaves (Montserrat et al. 2004), so is unlikely to be found on fruit. Nicholas Martin submitted that “Truss tomatoes are a group of ripe fruit still attached to their joint flowering stem. The stem is green and the fruit are attached by a green calyx. This makes the produce highly vulnerable to carrying quarantine pests such as tomato/potato psyllid. Because of the tomato/potato psyllid, truss tomatoes must be fumigated before export to most countries (Anon 2011). This application to release the mirid makes no mention of how this key pest is controlled and how this fits in with control of other pests and pathogens and how it would fit in with use of Macrolophus pygmaeus”. However, we understand that export tomatoes do not have any green material (T. Ivecevich pers. comm.), and that exporters are required to comply with Australia’s policy and apply protocols in the greenhouse, wash and brush fruit, and then fumigate prior to export. Truss tomatoes are being produced for the domestic market (T. Ivecevich pers. comm.). MPI have advised that “No species of Macrolophus (or its generic synonyms and Phytocoris), are listed in the Importing Country Phytosanitary Requirements (ICPRs) quarantine pest lists for Australia, China, Canada, Japan or New Caledonia. While some predatory species are listed in the ICPRs, there is no overarching reference to predatory species. However we have consulted the Imports Branch of the Australian Department of Agriculture and they have stated they would treat Macrolophus pygmaeus as actionable. This means they would fumigate, reship, or destroy the commodity on interception of M. pygmaeus. Further, if this predator was detected on a regular basis, compulsory fumigation or suspension of trade could be required, according to DAFF.”

3.71 Again, we assume that the industry is aware of these facts and still considers that the benefits outweigh any such costs. We therefore consider the effect of adverse impacts on our export markets to be negligible.

3.72 The wide range of prey fed on by M. pygmaeus does include E. formosa, a biological control agent widely used in New Zealand glasshouses. However, M. pygmaeus does not seem to disrupt whitefly control obtained through use of E. formosa (Castañé et al. 2004). On the basis of this information, and the ability of the industry to develop new best practice techniques, we do not rate this behavior as causing a significant effect.

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

Precautionary approach

3.73 Under section 7 of the Act, “all persons exercising functions, powers and duties under this Act,…shall take into account the need for caution in managing adverse effects where there is scientific and technical uncertainty about those effects.”

3.74 We consider that there is no scientific or technical uncertainty around this application. We recognise that there is an array of opinion around the severity of the adverse Figure 3 Scientific and technical uncertainty covers a effects and these appear to represent well-defined range of impacts, even where there may appear to be uncertainty on what those effects actually uncertainty, but we are confident that the are. The precautionary approach considers the uncertainty of any science outside that range. impacts fall within a well-defined range of risk (Figure 3). Any decision needs to be made according to how individuals view the importance of those risks.

Conclusion on adverse effects

3.75 After considering the available information, we consider that the adverse effects associated with the release of Macrolophus pygmaeus are non-negligible.

Positive effects

3.76 The applicant has identified potential positive effects on the environment, on society and communities, and on the market economy, associated with the release of Macrolophus pygmaeus. They consider that the release of M. pygmaeus has the potential to:  Make a crucial contribution to IPM in commercial vegetable production; and  Reduce the potential for human exposure to non-selective chemical sprays.

Human Health

3.77 The application is sparse on details as to the beneficial human health effects that could arise from the release of M. pygmaeus for use as a biocontrol in glasshouse, although they do state that “The main indirect benefit to human health from increased use of biological control agents is reduced reliance on non-selective chemical sprays.” The EPA considers that “OPCs [organophosphates and carbamates] affect the nervous system by inhibiting the enzyme acetylcholinesterase which leads to overstimulation of the nervous system. Of the two groups of substances organophosphates have a longer lasting effect on the nervous system than carbamates. OPCs are also harmful to the environment being very toxic to aquatic life and to terrestrial invertebrates, and in general they are also toxic to birds.” (EPA decision on the reassessment of OPC plant protection insecticides APP201045). However, the EPA found that methomyl and pirimiphos methyl, used in glasshouses to control whitefly and other pests,

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

presented low risk to operators and re-entry workers, and negligible risks to bystanders and the environment provided these substances are used in accordance with the controls.

3.78 In addition, a submission on that reassessment made by Nikki Johnson9; stated that with regards to dichlorvos, which did not form part of the EPAs reassessment, “….industry understands that the formulations of dichlorvos that are supported by the arable and horticultural industries are not under assessment in this application. Therefore no comments have been provided on the proposal for this compound. Industry strongly supports the continued use of this compound [emphasis added] and wishes to be involved in any consultation undertaken by EPA on potential changes”.

3.79 We have two things to consider in this case. Firstly, we consider that there is a direct conflict between the position expressed in the submission to the EPA on the use of dichlorvos in glasshouses, and the opinion expressed in the current application. The applicant for M. pygmaeus clearly states that “Assuming New Zealand growers could use BCAs with similar effectiveness to those utilised successfully by the Dutch greenhouse tomato industry then it is possible sprays for whitefly could be virtually eliminated within three years”.

3.80 John Thompson, who works to provide “technical back-up for crop production and crop protection for greenhouse crops in New Zealand” submitted on behalf of Bioforce Ltd. that “the majority of crops are reliant on chemical methods to control pests and this is neither good for the environment nor desirable for the people of New Zealand”. He considers that the value of IPM to society is paramount and that “When IPM programs fail, growers are forced to resort to chemical controls and large quantities of mostly hazardous chemicals are applied to our crops and food production areas annually. Nobody could successfully argue this is a safe practice as side effects may not be realised for many years after a new chemical is released even though extensive research is conducted before widespread use. However new chemicals are released in New Zealand every year and we simply do not know for sure what if any damage will ensue either as a direct effect of that chemical or in combination with others”.

3.81 Mike Sim submitted that [pirimiphos methyl and methomyl compounds] are “completely incompatible with bumblebees, and have residual impacts on beneficial insects for potentially several weeks”. We therefore consider that while the application is unclear on the mechanisms of IPM, there are people working in New Zealand who can advise the sector on an appropriate regime and who have a stated interest in reducing chemical use in glasshouses.

9On behalf of: The Foundation for Arable Research and the following Product Groups affiliated with Horticulture New Zealand; Avocado Industry Council, NZ Citrus Growers Inc, Persimmon Industry Council, Strawberry Growers NZ, Summerfruit NZ, Tamarillo Growers Assn, Onions NZ, Potatoes NZ, Process Vegetables NZ, Tomatoes NZ and Vegetables NZ.

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3.82 Secondly, we consider that the EPA has already assessed the risk from the use of pirimiphos methyl and methomyl compounds in glasshouses to workers or the environment outside glasshouses, as negligible to low. We therefore consider that any benefits derived from reducing the exposure to these chemicals could not be more than negligible to low.

3.83 However, although we have not finished the reassessment of dichlorvos, EPA staff have completed the risk assessment, and made it public, and we consider the risks from its use in glasshouses to be significantly greater than those from methomyl or pirimiphos methyl. The use of harmful chemicals risks public health, in particular to glasshouse workers and their families. These workers are vulnerable and the lack of engagement on their behalf in this application may suggest that they have little say in the chemicals they are exposed to, and instead simply bear the harm resulting from the provision of fresh tomatoes year-round.

3.84 If the tomato sector commits to finding alternatives to dichlorvos and can demonstrate that new IPM systems involving M. pygmaeus form part of that commitment, we consider that reducing the use of dichlorvos in glasshouses would constitute a significant benefit to the industry, local communities and potentially the wider New Zealand population. Peter Silcock submitted on behalf of Horticulture New Zealand that “the lack of availability of biocontrol agents such as Macrolophus does hinder achievement of these strategic outcomes [Hort Industry Strategy 2009-2020 - growing a new future]. This means that growers in NZ are controlling (usually non-native) pests using tools that are increasingly unacceptable to customers, consumers and regulators”.

3.85 We therefore consider the human health benefits to be non-negligible.

Economic

3.86 The applicant has stated that “IPM is an integral part of growers’ sales and marketing strategies”. Although domestic consumers are increasingly becoming aware of food safety, the real benefit of IPM is “perhaps more pronounced in the export markets”. They consider that “the economic benefits provided by the control of whitefly through the introduction of M. pygmaeus can be described in terms of reduced control costs, savings in yield and quality losses, and increased prices per kilogram achieved from more consistent production of premium fruit”.

3.87 In addition, they have provided a confidential appendix to the application, which detailed their in-house analysis of the value of introducing M. pygmaeus into their IPM programmes.

3.88 With the agreement of the applicant, under s58(1)(a) of the Act, we commissioned an independent report by the New Zealand Institute for Economic Research (NZIER) on the economic analysis presented in the application. Their review is available on the EPA website.

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3.89 In summary, NZIER stated that to be able to consider the economic benefits associated with the application, the applicants analysis would need to:  Stand-alone. This means setting out the full cost benefit analysis in line with comparable public policy questions; and  Compare and contrast the various options. One appropriate tool is a cost benefit analysis, which requires setting out:  the problem definition (as set out in the public application);  a brief context including the scale and significance of the issue at hand;  the options that should be considered;  the baseline or counterfactual that the costs and benefits are measured against;  the costs and benefits set out over an appropriate timeframe;  the discount rate (Treasury guidance suggests 8%);  the treatment of non-quantified costs and benefits;  the treatment of risk and uncertainty; and  conclusions based on the analysis.

3.90 We consider that while the applicant has defined the problem, and provided a context of the issue at hand, they have not outlined any options that they have considered (see Figure 1 of the NZIER report for an example of what we might have expected), or a baseline against which we can measure the economic benefits. In addition, they have not forecast their costs over an appropriate timeframe; NZIER suggested that 10 years would have been appropriate. As a result it is entirely possible that the applicant has underestimated the long term benefits (and costs) of their application. The opposite may also be true: despite Macrolophus, if growers have to keep spraying (for some other pest or disease) and these sprays are toxic to Macrolophus, then the economic benefits may have been severely over- estimated.

3.91 We consider that there are likely to be some economic benefits, albeit difficult to quantify with the information at hand, and that these benefits are likely occur at a local scale, where growers and large companies can expect to benefit from reduced spray costs. However, smaller growers acknowledge that IPM is expensive, and any significant economic benefits may not occur below a certain thresh- hold of growing capacity.

3.92 Mike Sim has submitted on behalf of Biobees Ltd., that they ”simply would not exist without greenhouse tomatoes, as their year round requirement for bumblebee hives allows us to keep bumblebees in continuous production, which is necessary for economic insect rearing”. This is an important consideration as it demonstrates the value to sectors and individuals not immediately related to tomato growing.

3.93 We therefore consider any economic benefits to be non-negligible.

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Conclusion on positive effects

3.94 Having evaluated the information, we consider that there are human health and economic benefits that can be accredited to the release of Macrolophus pygmaeus, and that these benefits are non- negligible.

The Effects on the Relationship of Māori to the Environment

3.95 The potential effects on the relationship of Māori to the environment have been assessed in accordance sections 6(d) and 8 of the Act. Under these sections all persons exercising functions, powers, and duties under this Act shall take into account the relationship of Māori and their culture and traditions with their ancestral lands, water, taonga and the principles of the Treaty of Waitangi (te Tiriti o Waitangi).

3.96 In consideration of these functions and duties, this section of the report will provide an overall evaluation of the consultation process with Māori that was undertaken by the applicant and highlight the matters arising from this. Commentary on submissions and the Ngā Kaihautū Tikanga Taiao report will also be provided as well as an assessment of the impact this application may have on the principles of the Treaty of Waitangi (Te Tiriti o Waitangi).

Consultation

3.97 Consultation with Māori is required to determine whether an application may have a significant impact on outcomes of importance to tangata whenua. This will include applications that potentially pose significant impact to:  Native or valued flora and fauna;  Sites of Māori cultural or other significance;  Environmental health and wellbeing generally;  Māori cultural practices and knowledge;  Māori social and economic wellbeing; and  Any statutory or other requirement or acknowledgement of relevance to the proposed activity.

3.98 Another purpose of Māori consultation is to provide the Decision Making Committee with sufficient information to evaluate risks, costs and benefits in order to make informed decisions in accordance with their legal duty under the Act.

3.99 To fulfil this requirement the applicant provided a presentation to the Māori National Network in 2012 on their then proposal to import and release three biological control agents; Delphastus catalinae, Nesidiocoris tenuis and Macrolophus pygmaeus.

3.100 Participant responses received from this presentation included concerns regarding the impact of the biological control agents to non-target species should self-sustaining populations establish outside of

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the intended areas of use; if the climate modelling was appropriate and accurate for this type of proposal; if there would be sufficient monitoring practices implemented by each user; and whether the application was consistent with the precautionary approach outlined in the Act.

3.101 In June 2013, the applicant also co-funded a Māori Reference Group (MRG) specifically established to support and identify potential adverse and beneficial effects of the application on the relationship of Māori to the environment. The MRG provided a report outlining their position and also numerous recommendations, however, at the time the reference group was established the proposal was to introduce three biological control agents and therefore some of the recommendations such as staggering the three releases no longer apply.

3.102 We note that the MRG have serious concerns about data gaps in the information provided to them at the time regarding the ability of M. pygmaeus to establish self-sustaining populations outside of the intended areas of use and the potential to seriously impact on native flora and fauna. They also suggest that if the application is successful that the end users be required to implement robust monitoring systems to minimise the risks of outbreaks occurring.

3.103 The MRG members also suggested that if the application was approved then the applicant update, or report back to, the EPAs Te Herenga (the National Māori Network) 12 and 24 months after release. It was reasoned that this measure would not only be an opportunity to update the MRG but also to support the work of kaitiaki in the regions in their role and obligation for managing the balance of species in the native environment.

3.104 Given the steps taken by the applicant we consider that the applicant has undertaken sufficient consultation to determine the impact of the proposal to Māori interests and also provide the decision making committee with sufficient information to evaluate risks, costs and benefits to Māori.

Submissions

3.105 Through the public submission process, the Ngāi Tahu HSNO Committee has provided comment on this application. They state while they generally support IPM regimes they oppose this application for several reasons such as the a lack of information in several areas; no testing carried out in regards to the impact on native plants or native prey species should self-sustaining populations of M. pygmaeus occur outside of the intended use areas; and also that a viable native alternative is available. Given these points, the Ngāi Tahu HSNO Committee considers that the active protection of their interests afforded to them under the Treaty of Waitangi and associated settlement legislation is not provided for.

Ngā Kaihautū Tikanga Taiao

3.106 Ngā Kaihautū Tikanga Taiao (NKTT) has also provided a separate report for the decision making committee’s consideration. They note the lack of New Zealand specific science and the risk of

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population establishment outside of the areas of intended use. NKTT also comment that iwi remain concerned about the constant push for more biological controls to be introduced which could ultimately have a compounding influence on ecosystems across New Zealand.

Impact on the Principles of the Treaty of Waitangi (Te Tiriti o Waitangi)

3.107 Under section 8 of the Act, all persons exercising powers and functions under the Act are to take into account the principles of the Treaty of Waitangi (te Tiriti o Waitangi). Under previously established case law (Bleakley v Environmental Risk Management Authority [2001] 3 NZLR 213, R v Westminster City (1990) and Haddon v Auckland Regional Council [1993]), the obligation to take into account is not intended to be higher than other relevant factors, but to give it whatever weight is appropriate in the circumstances, and if the appropriate matters have been to take into account then they must affect the discretion of the decision maker.

3.108 In reference to the “principles” of the Treaty of Waitangi, those currently accepted by the Courts and Waitangi Tribunal state them to be that of partnership, participation and protection.

3.109 The principles of partnership and participation refer to the shared obligation on both the Crown and iwi/Maori to act reasonably, honourably and in good faith towards each other to ensure the making of informed decisions on matters affecting the interests of Māori. In fulfilment of these principles, as previously stated, the applicant has completed a consultation programme including providing presentations and supporting a Māori reference group to comment on the proposed application.

3.110 The principle of active protection refers to the Crown‘s obligation to take positive steps to ensure that Māori interests are protected. Taking into account this principle requires the applicant to provide sufficient evidence to show that the introduction of M. pygmaeus does not pose a significant risk to native or taonga species, ecosystems and traditional Māori values, practices, health and well-being.

3.111 As highlighted in the previous section, Te Herenga members, MRG members, submitters and NKTT all note concerns around the ability of M. pygmaeus to establish an undesirable self-sustaining population. Based on the information assessed we consider that a self-sustaining population could form, however we do not consider that any population formed would trigger the minimum standards and would therefore not be classified as undesirable. Also, given the effectiveness of particular insecticides, it would be possible to eradicate small and localised populations.

3.112 Again, all groups noted concerns about the potential impact of M. pygmaeus to native flora and fauna. As stated previously, we have assessed the local impacts of M. pygmaeus in “natural habitats” and found that while negative consequences are possible these are unlikely to trigger the minimum standards.

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3.113 However, Māori may not agree with limiting the extent of our focus to merely “natural habitat” because it is inconsistent with the kaitiakitanga principle. This means that ultimately when taking into account the impacts on the relationship of Māori to the environment, the committee may need to consider a broader interpretation recognising that the integrity of native species in the entire environment is of concern to Māori. Therefore, from a Māori perspective negative consequences to flora and fauna are possible and will adversely impact on their ability to undertake kaitiaki responsibilities.

3.114 Finally, all groups note concern about the lack of information on M. pygmaeus in New Zealand specific environments. This data gap makes it difficult to draw further conclusions.

Conclusion on Effects on the Relationship of Māori to the Environment

3.115 Having evaluated the information, we consider that the principles or partnership and participation are provided for by this application. Given the potential adverse effects and significant data gaps we consider that the principle of active protection is not provided for by this application. Therefore we consider there are non-negligible effects on the relationship of Māori to the environment.

4 Weighing of adverse and positive effects

4.1 The HSNO Act and the Methodology require us to undertake a weighing of risks and benefits. To do this weighing we have separated risks and benefits into three scenarios: individual; local, and regional/national (Figures 4-6).

Individual scenario

4.2 The applicant has provided very little information pertaining to human health benefits to be realised from the release of M. pygmaeus. However, we consider that any reduction in the volume of harmful agrichemical used will have a non-negligible benefit to glass house workers.

4.3 We consider that the applicant has provided Figure 4 Risks to the environment in the immediate sufficient information to indicate that there is a non- vicinity of a glasshouse are negligible, while human health benefits to be gained through reducing OPC negligible economic benefit to the growers. applications are likely. Benefits therefore outweigh risks at this scale. 4.4 We consider that in the individual scenario it is clear that the benefits outweigh risk, although the balance of benefits in this scenario is carried by benefits to human health (Figure 4).

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Local scenario

4.5 We consider that there is a non- negligible benefit to the families of workers from any increased health benefits to the workers in tomato glasshouses. We also consider that a reduction in harmful chemicals like dichlorvos will benefit the health of New Figure 5 Risks to the modified environment surrounding glasshouses are non-negligible, and economic benefits are also Zealanders in general. non-negligible. Benefits are likely to outweigh risks at this scale. 4.6 We consider that there is a non- negligible economic benefit to business that support the tomato glasshouses, like Biobees and Bioforce. These businesses rely on the ongoing function of the industry to sustain their livelihoods.

4.7 We consider that there is a non-negligible risk that M. pygmaeus could damage crops in and outside of glasshouses and interfere with other biological control programs. However, we expect the industry has accounted for these risks when deciding whether to make their application to the EPA.

4.8 We therefore consider that in the local scenario benefits outweigh risks, although the balance of benefits in this scenario is carried by benefits to the economy of the industry (Figure 5).

Regional/national scenario

4.9 We consider that the models presented by the applicant underestimate the potential distribution of suitable climates and habitats for M. pygmaeus. We therefore consider that M. pygmaeus is likely to establish, at least in some parts of New

Zealand, and possibly widely.

4.10 We consider that there are some

species of plants, both native and introduced Risk Benefit (unquantified) to New Zealand, that could act as host

Risk / Benefit Risk plants for M. pygmaeus. However, we do not consider that M. pygmaeus will cause any significant damage to populations of these Figure 6 Risks to the environment at a regional/national scale plants, and therefore consider this effect to are non-negligible, while benefits at this scale are unquantified. Benefits therefore do not outweigh risks in this scenario be negligible.

4.11 We consider that M. pygmaeus predates on a range of prey species, both native and introduced. We consider this risk to be non-negligible.

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4.12 The applicant has not demonstrated human health benefits at a national scale; nor have they demonstrated the economic benefit at this scale. In this scenario, we consider that the risks are non- negligible and that there is no information on regional benefits. Therefore, we consider that in the regional scenario, we cannot demonstrate with the current information that benefits outweigh risks (Figure 6).

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5 Recommendation

5.1 In the submissions that were received on this application, there are two predominant and opposite views expressed. One where New Zealand needs to embrace safe food production, even if this means being exposed to some anxiety over the environmental effects; the other that the state of the environment must be preserved and any information gaps must mean a decline.

5.2 Section 5(b) of the Act requires that we recognise and provide for “the maintenance and enhancement of people and communities to provide for their own economic, social, and cultural well-being and for the reasonable foreseeable needs of future generations”. In declining this decision, we limit the options available to the production sector, and we can expect the continued use of harmful agrichemicals in their pest management programmes. In short this will result in taking a ‘do nothing’ approach. The industry will be able to say that there are no viable alternatives to harmful insecticides and the reliance on such chemical inputs will continue.

5.3 The applicant has not demonstrated any long term regional/national benefits, including economic or human health benefits, however there is a clear risk to native fauna. We remain uncertain as to the exact outcome that the industry is attempting to achieve. The application implies that biological control and hence M. pygmaeus is critical to the survival of the industry and that they intend to reduce their dependence on chemical means of pest control. Unfortunately, there is little practical evidence that supports such an interpretation.

5.4 In making our recommendation, along the lines of section 5(b) of the Act, we consider the decision must be made by weighing regional/national long term environmental risks against long term regional/national benefits.

5.5 We therefore recommend that this application be declined.

Asela Atapattu Manu Graham Kate Bromfield Manager Senior Advisor Senior Advisor New Organsims Māori and Policy New Organisms

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Appendix 1A. Professor Jeff Bale CV

PERSONAL DETAILS

Name: Jeffrey Stuart Bale

School: Biosciences

Title of Chair: Professor of Environmental Biology

Date of appointment: July 1992

UNIVERSITY EDUCATION AND DEGREES AWARDED

1968-1973 BSc in Agricultural Zoology, Class I, University of Newcastle upon Tyne (includes sabbatical year as President of the Student’s Union)

1977 PhD ‘Aspects of the behaviour and biology of the beech leaf mining weevil, Rhynchaenus fagi L’. University of Newcastle upon Tyne

CAREER SINCE GRADUATION

1976-1978 University Fellow: Lord Adams Fellowship. University of Newcastle upon Tyne

1977-1978 Temporary Lecturer in Agricultural Zoology. University of Newcastle upon Tyne

1979-1981 Junior Lecturer in Agricultural Zoology. Department of Pure & Applied Zoology. University of Leeds

1981-1988 Lecturer in Crop Entomology. Department of Pure and Applied Zoology. University of Leeds

1987-1988 Nuffield Science Research Fellow (Sabbatical)

1988 Visiting Scholar: Department of Biological Sciences. State University of New York. Binghamton USA

1988 Senior Lecturer in Crop Entomology. Department of Pure and Applied Biology. University of Leeds

1992 to date Professor of Environmental Biology. School of Biological Sciences. The University of Birmingham

2007 Visiting Professor, University of Rennes

2008 Director of Quality Assurance and Enhancement. College of Life and Environmental Sciences. University of

Birmingham

2009 Deputy Pro-Vice-Chancellor (Education). University of Birmingham

2013 Pro-Vice-Chancellor (Education). University of Birmingham

MAJOR RESEARCH INTERESTS

My major research interest focuses on the thermal biology of invertebrates, particularly insect and mites. From an initial emphasis on the physiological aspects of the main mechanisms of insect survival at low temperature (by freeze tolerance or avoidance), this interest has developed in several related areas, such as an expanded and more ecologically relevant classification of strategies of cold hardiness, adaptations for life in extreme environments (including research expeditions to the Arctic and Antarctic), responses to climate warming,

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and most recently, assessing the establishment potential and impacts of non-native biocontrol agents. Much of this research has tried to

‘bridge the gap’ between ecology and physiology.

CAREER ACHIEVEMENTS

I have held 35 research grants, supervised over 50 PhD students and published over 200 papers. In relation to biological control and the risk assessment of non-native species, I was a member of the UK government’s ‘Advisory Committee on Releases to the Environment’

(ACRE) for 10 years. I was the Convenor of the IOBC (WPRS) ‘Commission on the Harmonisation of Invertebrate Biological Control

Agents’ (CHIBCA), and the Principal Investigator for invertebrate biological control agents (IBCAs) in the EU-funded REBECA project

(Regulation of Biological Control Agents).

SELECTED PUBLICATIONS

Bale, J. S. and Walters K.F.A. (2001). Overwintering biology as a guide to the establishment potential of non-native arthropods in the

UK. In 'Temperature and Development' pp 343-354. Eds D. A. Atkinson and M. Thorndyke. Bios.

Hart, A.J., Tullett, A.G. Bale, J.S. and Walters, K.F.A. (2002). Effects of temperature on the establishment potential in the UK of the non- native glasshouse biocontrol agent Macrolophus caliginosus. Physiological Entomology 27, 112-123.

Hart, A.J., Bale, J.S., Tullett, A.G., Worland, M.R. and Walters, K.F.A. (2002). Effects of temperature on the establishment potential of the predatory mite Amblyseius californicus McGregor (Acari: Phytoseiidae) in the UK. Journal of Insect Physiology 48, 593-600.

Hatherley, I., Bale, J.S. and Walters, K.F.A. (2004) Thermal biology of Typhlodromips montdorensis: implications for its introduction as a glasshouse biological control agent in the UK. Entomologia Experimentalis et Applicata 111, 97-109.

Tullett, A.G.T., Hart, A.J., Worland, M.R. and Bale, J.S. (2004) Assessing the effects of low temperature on the establishment potential in Britain of the non-native biological control agent Eretmocerus eremicus. Physiological Entomology 29, 363-371.

Hatherly, I.S., Bale, J.S. and Walters, K.F.A. (2005) U.K. winter egg survival in the field and laboratory diapause of Typhlodromips montdorensis. Physiological Entomology 30, 87-91.

Hatherly, I.S., Hart, A.J., Tullett, A.G.T. and Bale, J.S. (2005) Use of thermal data as a screen for the establishment potential of non- native biocontrol agents in the UK. BioControl 50, 687-698.

Bale, J.S. (2005) Effects of temperature on the establishment of non- native biocontrol agents: the predictive power of laboratory data. Second International Symposium on Biological Control of Arthropods (IBSCA), Vol. II, 593-602.

Hatherly, I.S., Bale, J. S. and Walters, K.F.A. (2005) Intraguild predation and feeding preferences between three species of phytoseiid mite used for biological control. Experimental and Applied Acarology 37, 43-55.

Bigler, F., Bale, J.S., Cock, M.J.W., Dreyer, H., GreatRex, R., Kulhmann, U., Loomans, A.J.M. and van Lenteren, J.C. (2005) Guidelines for information requirements for import and release of invertebrate biological control agents in European countries. Biological Control

News and Information 26, 115-123.

Boivin, G., Kölliker, U., Bale, J.S. and Bigler, F. (2006). Assessing the establishment potential of inundative biological control agents. In

'Environmental Impact of Invertebrates for Biological Control of Arthropods: Methods and Risk Assessment'. Eds F. Bigler, D.

Babendreier and U. Kuhlmann. CABI.

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Hatherly, I.S., Pedersen, B.P. and Bale, J.S. (2008) Establishment potential of the predatory mirid in northern

Europe. BioControl 53, 589-601.

Bale, J.S., Allen, C.M and Hughes, G.E. (2009) Thermal ecology of invertebrate biological control agents: establishment and activity.

Third International Symposium on Biological Control of Arthropods (IBSCA), 56-65.

Hatherly, I.S., Pedersen, B.P. and Bale, J.S. (2009) Effect of host plant, prey species and intergenerational changes on the prey preferences of the predatory mirid Macrolophus caliginosus. BioControl, 54, 35-45.

Hughes, G.E., Sterk, G. and Bale, J.S. (2009) Thermal biology and establishment potential in temperate climates of the predatory mirid

Nesidiocoris tenuis. BioControl 54, 785-795.

Berkvens, N., Bale, J.S., Berkvens, D., Tirry, L. and de Clercq, P. (2010) Cold tolerance of the harlequin ladybird Harmonia axyridis in

Europe. Journal of Insect Physiology 56, 438-444.

Bale, J.S. (2010). Regulation of invertebrate biological control agents in Europe: recommendations for a harmonized approach. In

‘Regulation of biological control agents in Europe’, pp 323-373. Ed. R. Ehlers. Springer.

De Clercq, P. and Bale, J.S. (2010). Benefits and risks of biological control – a case study with Harmonia axyridis. In ‘Regulation of biological control agents in Europe’, pp 243-255. Ed. R. Ehlers. Springer.

Hughes, G.E., Owen, E., Sterk, G. and Bale. J.S. (2010) Thermal activity thresholds of the parasitic wasp Lysiphlebus testaceipes: implications for its efficacy as a biological control agent. Physiological Entomology 35, 373-378.

Hughes, G.E., Sterk, G. and Bale. J.S. (2011) Thermal biology and establishment potential in temperate climates of the aphid parasitoid,

Lysiphlebus testaceipes. BioControl 56, 19-33.

Bale, J.S. (2011) Harmonisation of regulations for invertebrate biocontrol agents in Europe: progress, problems and solutions. Journal of

Applied Entomology 135, 503-513.

Coombs, M.R. and Bale, J.S. (2013) Comparison of thermal activity thresholds of the spider mite predators Phytoseiulus macropilis and

Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseiidae). Experimental and Applied Acarology 59, 435-445.

Coombs, M.R. and Bale, J.S. Thermal biology of the spider mite predator Phytoseiulus macropilis. Biocontrol (in press).

Coombs, M.R. and Bale, J.S. Thermal thresholds of the spider mite predator Balaustium hernandezi Von Heyden (Acari: Erythraeidae).

Physiological Entomology (in press).

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Appendix 1B. Comments provided by Professor Jeff Bale

General comments

The report is well written and researched. The conclusions are balanced and evidenced-based. The report correctly identifies information that has either, not been fully considered by the applicant, or in some areas, largely ignored.

Whilst the report concludes that the application should be declined, I feel that the grounds for this recommendation could have been more clearly articulated, and as a result, this recommendation made with greater power. In essence, (i) there is evidence that Macrolophus pygmaeus has established in climatic areas similar to New Zealand (UK), can survive through winter in such climates, and CLIMEX modelling predicts establishment in some parts of New Zealand post-release; and (ii) M. pygmaeus is polyphagous and predates a range of arthropod taxa that are part of New Zealand’s native fauna. The question I would therefore pose is under what circumstances would the relevant New Zealand authorities consider that a case could be made for release. My comment here is whether a brief summary of the reasons for the recommendation to ‘decline’ should be included in Section 4 (page 37), as the current text implies that if a stronger case was made for the benefits of release, a different recommendation could have been made. Is that really true, given the near certainty of establishment and likely effects on non-target organisms (NTOs)?

Executive Summary (ES)

Para 1

I note the emphasis on IPM. I wonder whether it may be useful to add a comment to the effect that biocontrol, or the inclusion of biocontrol as part of IPM, often arises when other methods of control have become less effective (e.g. pest has developed resistance to chemical control), or no other control is available. It would also be helpful to make clear that the applicant is seeking to release M. pygmaeus into glasshouses (and perhaps other contained facilities) and the risk assessment contained within the report seeks to determine whether escapees from such environments are likely to establish outdoors and as a result, pose a threat to New Zealand’s native flora and fauna.

Para 3

I am not familiar with ‘clause 27 of the Methodology’, and nor would anyone not familiar with the New Zealand regulatory processes. I think the ES needs some brief legislative context, as is found in Section 1. For example, under which act in New Zealand are applications made to release non-native biocontrol agents (presumably HSNO?); and what is ‘the Methodology’, and the content of ‘clause 27?

When the risks to human health are discussed in relation to biocontrol, this is usually in terms of allergies suffered by workers in natural enemy production facilities. My interpretation of this paragraph is that the applicant is claiming possible benefits of IPM/biocontrol resulting from the reduced use of pesticides. This needs to be made clear, even if the case itself has not been well made.

Section 1

Para 1.2

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For my profile and after ‘thermal tolerances of insects’, please insert ‘the risk assessment of non-native biocontrol agents’, ‘and has worked extensively……….’.

Para 1.11

Whilst it is true that no ‘active host range test trials’ have been conducted by the applicant, there have been many studies elsewhere that have indicated the polyphagous nature of M. pygmaeus, and many of these reports are set out in Table 2 (pages 52-53); a statement to this effect could be added to this paragraph.

Para 1.14

I would only note in passing that this is a good description of the situation, including the possible impacts of changes in European pesticide legislation on the options for chemical control.

Para 1.16

As far as I am aware both the regulatory framework for the import and release of non-native biocontrol agents, the cool temperate climate, and the glasshouse pests affecting tomato production, are similar between New Zealand and the UK, so it may be worthwhile to compare options for control between these two countries.

Para 1.18

I think there is acknowledgment that tomato can be a difficult crop on which natural enemies can operate because of their trichomes (defence strategy).

1.21

A minor point of clarification here – glasshouse whitefly can disperse in the winged adult stage and in the early nymphal instars, but the later instars are increasingly immobile.

Section 2

Para 2.2

This description of previous taxonomic confusion is correct.

Para 2.4

Some care is required in considering other countries where M. pygmaeus has been commercially released. Firstly, some EU countries have no regulation on the release of non-native biocontrol agents, and in other countries, M. pygmaeus was released prior to the introduction of more stringent regulations. For example, it is true that M. pygmaeus has been released in UK glasshouses for the control of glasshouse whitefly. However, these releases date back to 1995 and prior to the introduction of the risk assessment protocol now in place. If an application for release had been submitted recently and with the knowledge that the species can survive through winter (Hart et al., 2002) and predate, develop and reproduce on NTOs (Hatherly et al.,2009), in my ‘expert’ opinion, the species would not receive a release licence.

Section 3

Para 3.6

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This is an important paragraph in a number of respects. Firstly, the applicant’s own CLIMEX modelling predicts some establishment in New Zealand. Whilst the accuracy of this modelling technique and its interpretation can be questioned, it seems to beg a wider question: is any level or locality of establishment of a non-native species acceptable?

Secondly (and this also relates to para 3.7), the CLIMEX data and habitat matching are ‘proxy’ measures for likely establishment but are no substitute for a direct assessment of overwintering ability carried out under quarantine conditions. If the New Zealand authorities allow such assessment, this would provide a more reliable assessment of establishment potential.

Para 3.10

I agree with the comment that the earlier taxonomic confusion around the three Macrolophus species raises some doubt about the applicability of the CLIMEX data, and any assumptions concerning the ecophysiology and thermal tolerances of the species.

Para 3.11

Also agree with this conclusion on the risks of predicting establishment from CLIMEX modelling alone.

Para 3.15

I think this paragraph contains important information that is rooted in the theory of invasion biology. If there are repeated intentional releases of a species then establishment is more likely to occur where the species has the potential to do so. This is clearly the case with M. pygmaeus.

There is a further dimension to establishment potential. Biocontrol companies refresh their production cultures with ‘fresh wild caught’ material (to maintain genetic diversity), hence there is a risk that over time, the commercially released organisms may have different ecophysiological properties compared with earlier stock, especially if the refreshed material is collected from different locations.

Para 3.17

I do not have a specific comment on this paragraph, but rather, the ordering of information that makes up the risk assessment. Joop van Lenteren, Franz Bigler and myself have published a ‘risk assessment protocol’ (see slide 1 attached) that recommends testing in the order of establishment, host range and dispersal. This would be the default order, especially in the case of a release of a non-native species into a glasshouse-only environment and in a climate where there is a winter season that might act as a natural barrier to outdoor establishment – such as the situation with M. pygmaeus in New Zealand. If this protocol is followed and overwintering tests show that all life cycle stages die out after 2-4 weeks in the field, then there is no risk of establishment. In this situation it would not be necessary to carry out tests on host range, because in the absence of establishment, there could be only limited impact on native NTOs.

This approach also highlights a further principle: summer-only outdoor establishment has to be accepted, for glasshouse biocontrol to be viable i.e. a conservation-based objection to summer-only establishment should be rejected if the alternative is chemical control. But, this situation is different, as ‘permanent’ establishment seems likely.

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Para 3.19

The main comment here is on the use and definition of terms. There is a statement and a reference that M. pygmaeus can ‘survive on many plants’ (Table 1) and ‘utilise a wide range of prey’. Distinction needs to be made between ‘surviving, utilising, predating’ various plants and prey, and being able to develop on those food sources i.e. moult through the instars to adult; and being able to reproduce and sustain a viable population. In terms of risk, simply ‘predating’ a NTO is less of a problem if the agent cannot develop or reproduce on the prey.

I am attaching a slide of data from Hatherly et al., (2009) that indicates that M. pygmaeus can feed, develop and reproduce on NTO species over 3 generations, which highlights the risk of establishment beyond the inherent cold tolerance and overwintering ability (see slide 2 attached).

Para 3.24

The line of argument in this paragraph is correct; but note also that a mobile predator with access to prey does not have to survive outdoors through an entire winter; individuals can exploit intermittent warmer conditions to move to more sheltered locations e.g. back into a glasshouse.

Para 3.25

Note that as indicated above, I would move this paragraph(s) to earlier in the risk assessment.

I agree that outdoor establishment is likely – it is predicted by the CLIMEX modelling. I would have welcomed some direct assessment of overwintering ability. Also, note the comment about the natural variation in ecophysiological parameters in commercial breeding stock, and how this can change with ‘refresh material’.

I think it is legitimate to suggest that there is some discussion about the implications of climate change, although, as establishment is predicted under the current climate, any increase in temperature might be expected to favour further establishment and/or the area over which such establishment occurs.

Para 3.26

Second sentence needs checking.

Para 3.27 (and other paragraphs in this section)

I think the key point to emphasise here is that studies on host range are essential for M. pygmaeus because establishment is predicted. If there was no published information available, host range tests should have been conducted by the applicant. As it is, there is substantial published data available.

This may also be the place to emphasise the distinction between predation, development and reproduction. Whilst it would undoubtedly be regarded as undesirable for a non-native biocontrol agent to feed on a rare native (insect) species, the impact of this predation would be greater in the longer term if the agent could establish a sustainable population via NTOs more generally. The data of Hatherly et al., (2009) are particularly relevant to this section. Macrolophus caliginosus (but later confirmed as M. pygmaeus) were provided with the target prey (Trialeurodes vaporariorum), a related species (Cabbage whitefly Aleyrodes proletella) and an unrelated species, the aphid Myzus persicae. Macrolophus pygmaeus fed,

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

developed and sustained a population on all three prey species (see slide attached). An important point here is that aphid species with anholocyclic (asexual) clones are available as prey throughout winter.

Para 3.36

The polyphagous nature of M. pygmaeus with regard to plant hosts adds a confounding factor to its similarly polyphagous utilisation of arthropod prey. I think this paragraph reflects the view of the DOC and particularly the comment of De Clercq (2011) that generalist (polyphagous) predators and parasitoids pose a risk in biocontrol, especially with regard to non-native species that are likely to establish outside of the release environment.

Paras 3.41 - 3.43

I think that all the text in these paragraphs is relevant, though I would note that impacts on native arthropod fauna may be more important. The zoophytophagous nature of M. pygmaeus is relatively rare.

Paras 3.50 and 3.51

I agree with these conclusions.

Para 3.54

I do not agree with this conclusion. Evidence suggests that some non-native biocontrol agents released into glasshouses establish outdoors (e.g. the mite Neoseiulus californicus and M. pygmaeus in the UK), but if there is no post-release monitoring or obvious impact, populations can build up undetected, but then be impossible to eradicate with insecticides. I am not confident that even with small, localised populations, that eradication could be guaranteed.

Para 3.60

Two minor points, in the second line, there should be a comma after ‘are possible’, not a semi-colon. Also ‘Bale et al. 2011,is not in the reference list.

Para 3.61

Naturally occurring native predators are strictly speaking ‘natural control agents’ (not biological control agents).

Para 3.106

See earlier comments. In my view, given the overwintering ability of M. pygmaeus coupled with its polyphagous predatory nature I feel that establishment outdoors is likely and I less certain that eradication with an insecticide could be guaranteed.

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

Para 3.111

A good summary of the different views.

Para 3.125

I do not agree with this view which seems a rather weak statement. There are two key findings from the risk assessment. Firstly, it is almost certain that M. pygmaeus would establish outdoors after repeated releases into glasshouses. Secondly, there would be a wide range of plant and arthropod food resources/prey available to M. pygmaeus. Faced with this information, would an environmentally responsible tomato industry still seek a licensed release of M. pygmaeus?

I note the reference in para 1.11 to tests on 10 arthropods as potential biocontrol agents for the glasshouse industry. Was M. pygmaeus the only natural enemy of glasshouse whitefly investigated?

In para 3.94 there is a reference to Delphastus catalinae and Nesidiocoris tenuis. My laboratory has investigated the establishment potential of both of these species as well M. pygmaeus (see attached slides 3 and 4). We have identified a robust relationship between survival in the laboratory at 5⁰C and the duration of survival in the field in winter. This predictive relationship shows that whilst M. pygmaeus (californicus) is not the most cold hardy species (in comparison with Neoseiulus californicus and Dicyphus hesperus), it can survive through a UK winter. By comparison, there are a cluster of weakly cold tolerant species that die out in the field within 2-4 weeks, including Delphastus catalinae and Nesidiocoris tenuis.

In the attached slide 4, ‘risk of establishment’ categories have been placed around different species. Macrolophus pygmaeus is slightly above the ‘medium risk’ category, reflecting its ability to survive for relatively long periods of time in UK winters.

Overall conclusion

If M.pygmaeus was released into New Zealand glasshouses, individuals would escape into the surrounding environment and most likely establish self-sustaining populations. I do not believe that such populations could be subsequently eradicated. The potential threat to New Zealand’s native arthropod fauna is unknown.

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

Figure 7 Slide 1 referred to in comments by Professor Bale

Figure 8 Slide 2 referred to in comments by Professor Bale

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

Figure 9 Slide 3 referred to in comments by Professor Bale

Figure 10 Slide 4 referred to in comments by Professor Bale

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

Appendix 2 Summary of Submitters

Submission Submitter/ Support/ Submitter comments organisation Oppose

108116 Nursery and Garden Support  Happy that any concerns Nursery and Garden Industry New Industry New Zealand Zealand have will be addressed by the process the EPA follows

 Does not anticipate any impacts on Nursery production in New

Zealand

 Recognises the possible benefits provided

 The nursery industry suffers from greenhouse whitefly thus there

may be some minor benefits from the proposed release

108117 Rembrandt van Rijen Support  Growers are struggling with control of whitefly and tomato psyllids in Ltd. greenhouses

 Winter growers cannot depend on Encarsia and are reliant on

sprays

 Growers are facing chemical resistance issues with white fly

 Macrolophus has almost eliminated the need for chemical usage in

Europe

 Approving the application is a critical component of the industries

‘Integrated Pest Management’ programme

108118 Kovati- Tam Yam Support  Reduces reliance on agri-chemicals Gardens  Good for the environment, consumers and growers

108119 Karamea Tomatoes Support  Tomato growers do not have enough products available to control Limited whitefly

 Whitefly is becoming resistant to many sprays currently in use at

their complex

 Use of biological control agent preferable to sprays

108120 Bhupinder Singh Gavri Support  Reduce the reliance on agri-chemicals

 The use of M. pygmaeus should be affordable and if possible

subsidised

108121 Great Lake Tomatoes Support  Macrolophus will provide an alternative for controlling whitefly Limited  Macrolophus can destroy up to 50 whitefly eggs a day  Encarsia alone is not an option to combat whitefly effectively

 Some chemicals will damage the bumble bees that pollinate the

flowers

 Applying chemicals causes mechanical damage to plants and fruit,

diminishing its value

 There is potential to effectively fight whitefly as well as other bugs

with the combination of Macrolophus and Encarsia alone

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

Submission Submitter/ Support/ Submitter comments organisation Oppose

 Macrolophus is a very sensitive creature that will very likely die

outside the protected environment a glass house provides

 Macrolophus will be brought into an ideal environment where food

is plenty so migration outside the glass house will be very small

 The risks are very limited  The financial and environmental benefits can be massive

108122 Gourmet Mokai Limited Support  Sprays used for whitefly control are limited  Insect resistance to sprays will become an issue

 Encarsia is not effective due to New Zealand’s summer climate

 M. pygmaeus is proven to be effective predator of whitefly in other

countries with similar climate to New Zealand

108123 EM & DC Duncan Support  Wishes the EPA to allow M. pygmaeus for the control of whitefly in

greenhouse tomatoes

108659 Nicholas Martin Oppose  No information is provided to show how M. pygmaeus will be used

in IPM

 Claims of financial benefit are false

 M. pygmaeus can cause damage to plants  May endanger biological control agents introduced to control weeds

and disrupt biocontrol in other crops, thus increasing the need for

pesticide sprays

 May compete with native predatory insects

108666 Landcare Research Oppose  Expect M. pygmaeus to escape glasshouses  Consider M. pygmaeus could establish outside glasshouses

 Believe it could disperse to potentially vulnerable native plants

 Recommend surveys of potentially vulnerable plants  Concerned about other biological control programmes, especially

against woolly nightshade as the agent already has its efficacy

reduced by predation

 How would current control methods for TTP affect Macrolophus?

 Committed to biocontrol and not fundamentally opposed to

generalists but would prefer to see use of those that cannot survive

outdoors

108668 Northland Regional Concerned  There will be benefits from reduced insecticide use Council  Existing predator/prey relationships may be affected

 Further host testing required

108673 Wilderness Trappers Concerned  The application does not consider the effects of climate change

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

Submission Submitter/ Support/ Submitter comments organisation Oppose

 Native BCAs for control of greenhouse whitefly should be

considered

109392 Margaret Hicks Oppose  Doubt over claims export markets are primary consumers?

Requests trade figures to support the claim

 Whitefly infestation results from unnatural growing conditions

 Large scale operations facilitate the spread of pests

 Cease year round production as cold spells help control pests  Promote companion planting

 Applicant hasn’t accounted for climate change

 Tomato growers have no right to put native insects at risk  Precautionary approach essential

109397 Anthony Tringham Support  Need more biocontrols to control pests  Growers do not want to rely on chemical controls

 Before TPP, most pest control was done by biocontrol agents

109398 Entomological Society Oppose  No assessment of potential predators already present in New of New Zealand Zealand that could be used for the control of whitefly using

inundative biocontrol

 Agree that CLIMEX modelling indicates that only certain regions of

New Zealand are likely to support populations outside of a

greenhouse environment

 Insufficient information to ascertain the spatial extent of risk

 The economic assessment does not include the potential export

phytosanitary complications of introducing M. pygmaeus

 May impact on existing biological control programmes

109418 Abma Hothouse Support  Let us use Macrolophus to manage whitefly Tomatoes

109419 Fausett Partnership Support  Cost and potential damage caused by whitefly

 Spraying is costly and bad for the environment  A natural, efficient alternative is good for industry

109420 S. McCulloch Support  Whitefly is prolific and there are not a lot of options for control other

than chemicals

109409 New Zealand Farm Oppose  Support biocontrol targeting insect pests Forestry Assn.  Concern around the damage or disruption to existing biocontrols

 No documented evidence that existing whitefly predators are not

effective augmentative control agents

 Concerned around the accuracy of the models and expect that

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Submission Submitter/ Support/ Submitter comments organisation Oppose

Macrolophus could actually through most coastal areas in New

Zealand

109410 Margaret Stanley Oppose  M. pygmaeus is a generalist predator

 High probability of significant effects on natural ecosystems

109411 Tony Norton Support  Encarsia does not cope well with high pest pressures

 Chemicals used for whitefly are the same as those used for TPP  To avoid chemical resistance, sprays can only be used 2-3 times

per year

 Customers demand spray free  Staff are sensitive to sprays and residue

109412 Janet Taiatini Oppose  Introduction is not in the best interests of biodiversity  Applicant has not presented comprehensive risk analysis

109413 Kingbridge Ltd Support  Good bugs will be good for the health of staff and customers, and

save time, labour and money

109408 Ngai Tahu Oppose  Consider there is a viable native alternative (hook-tipped lacewing)  In general, support IPM and reduced spray use

 Treaty of Waitangi responsibilities serve to protect native

environments

 Economic assessment probably minimal at best but as it was

deemed confidential, “who knows”

 Airfreighting low value perishables unsustainable

109417 Bioforce Support  IPM is a must do practice to ensure sustainable crop protection

 Multiple controls are needed for each pest  Beneficial generalist arthropods have important benefits

 Biocontrol is the only responsible and sustainable option for pest

control

 New Zealand cannot afford to be locked into ongoing chemical

control for important pests

109416 Biobees Support  Bees are at risk from OPCs used in glasshouses

 Bumblebees are essential for tomato pollination

 M. pygmaeus could be used to control other glasshouse pests like

TPP

109415 Horticulture NZ Support  Genuine desire to provide consumers with the safest, highest

quality product possible

 Use of biocontrol agents requires growers to be skilled in crop

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

Submission Submitter/ Support/ Submitter comments organisation Oppose

management

 Benefits are reduced or no spray residues, improved quality and

production, and lower production costs

109414 NZ Biosecurity Institute Oppose  Do not consider that Macrolophus will be contained in glasshouses  Believe Macrolophus could establish in New Zealand

 A range of non-native plants i.e. wooly nightshade, a widespread

weed, could act as host

 Insufficiant information available assess the risks to native plants

 Introduction could compromise biocontrol programme for wooly

nightshade

 No information about TPP

 The greenhouse industry is small and we cannot assess economic

impacts

 Fundamentally not opposed to the use of a generalist in biocontrol

programmes, but need safety to be more rigorously demonstrated

109421 Dirk Bier Support  Macrolophus can save $66,000 per hectare per year and is

important to ongoing profitability of the industry

109422 Diana Ellingham Support  Grow organic vegetables and support introduction of species that

reduce sprays

 Whitefly is a major pest at times

109454 David Price Support  Whitefly is a real problem

 Macrolophus will reduce sprays

109455 Pierre Gargiulo Support  Markets demand no spray residue

 Costs increasing and value return per kilo less than it was 10 years

ago

 Need to reduce spray costs and think Macrolophus will help do this

 Limited control options

109458 Geoff Lamont Support  The Dutch are achieving good whitefly control with Macrolophus

 We spray regularly to control whitefly and thrips

109460 Tony Boyd Support  Advantages of IPM include safer work environment and less

chemical residue

 Few control options for whitefly so growers must spray

109589 Won Ha Park Support  Macrolophus widely used in glasshouses overseas  Reducing reliance on agrichemicals is good for the environment

 Increases growers choice in pest management

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Application for approval to import and release Macrolophus pygmaeus (APP201254)

Appendix 3 Comments from DOC DOC comments on EPA new organism for release application

7th February, 2014

Application number: APP201254

Applicant: the greenhouse tomato industry, represented by Tomatoes New Zealand (TNZ)

Application purpose: To import and release Macrolophus pygmaeus, a polyphagous, predatory mirid from the Mediterranean, as a biocontrol agent for the control of greenhouse whitefly and other pests of greenhouse tomatoes

Submission period closes: 7 February 2014

Thank you for the opportunity to comment on this application. Please note we wish for Chris Green, the Department of Conservation’s Technical Advisor Threats (entomology), to speak at the public hearing in support of the Department’s comments. Accordingly, please advise us of the hearing date and location.

Whilst the Department recognises the greenhouse tomato industry’s (represented by Tomatoes New Zealand [TNZ]) intention is to import and release Macrolophus pygmaeus as part of an integrated pest management approach to maintain greenhouse whitefly (Trialeurodes vaporariorum) at acceptable levels and reduce the use of insecticides into the environment, we do not believe the specific risks posed to New Zealand’s native biota have been adequately identified, assessed or mitigated by this application. Accordingly, we do not support the new organism release of Macrolophus pygmaeus into the New Zealand environment. We request the EPA decline this application. Assessment of risk to conservation values

TNZ’s conclusion that M. pygmaeus will not pose a risk to the NZ environment is largely based on their conclusion that the organism will not be able to form self-sustaining populations in habitats supporting native host species. This conclusion was drawn from taking into account the organism’s thermal biology requirements, CLIMEX and habitat modelling outcomes and day length impact on fecundity.

The consensus multimodelling suggests that M. pygmaeus could be restricted to a small area north of Kaitaia if it established; but the CLIMEX modelling indicates that suitable climate conditions may also exist north of Hamilton, large areas of coastal North Island, particularly the east coast, as well as coastal Marlborough and Nelson. There appears to be considerable disparity between the two modelling methods used. We note that Logan et al. (2013) in Appendix 9.6 states that due to the small sample size of training datasets (N=23) for Macrolophus spp the model performance is likely to be compromised. They further advise caution in the interpretation of the results of the Maxent and Multi Models in particular and indicate the CLIMEX results may be more reliable. We therefore believe the assertion that M. pygmaeus will be unable to form self-sustaining populations in the wild is flawed and certainly does not justify its introduction. We note that following its introduction to the UK in 1995 M. pygmaeus (= M. calignosus = M. melanotoma ) was unexpectedly found to be surviving outside greenhouses during winter and predicted to be able to complete two generations a year (Hart 2002). This could indicate an ability of the species to

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colonise new climatic environments beyond those initially predicted. The extent to which the UK distribution records and their climatic data were used in the Multi Models is unclear.

The application attempts to make a case for M. pygmaeus being unable to survive in the wild except for restricted areas based on environmental parameters, particularly ambient temperature. With the reliance on temperature we would have expected a discussion on the potential, if not actual, effects of climate change on distribution limits. However, there is no reference or discussion on this at all. Climate change, as a real phenomenon, is increasingly being accepted by the world’s scientific community. Its affect on New Zealand’s climate would, in all likelihood, lead to an increase in the potential distribution of M. pygmaeus beyond the areas indicated by the modelling in the application.

The applicant has also indicated that it would be less likely for M. pygmaeus to establish in the area north of Kaitaia, as there are no tomato greenhouses currently in the area to provide source insects. This assertion is misleading on two points: first the application maps (in Appendix 9.8) only the “main tomato greenhouse locations”, disregarding other potential present greenhouses and future greenhouse development, and second the application fails to appreciate there will be numerous exotic hosts for M. pygmaeus present that would likely form a link between greenhouse facilities and native hosts in native habitats. Consequently, the greenhouses specific locations are irrelevant.

Given there is the potential for M. pygmaeus to establish within the New Zealand environment, it is necessary to consider the impacts to the native biota within the vulnerable locations; particularly those areas described as “optimal” north of Auckland and the east coast of the North Island. Native invertebrate fauna

M. pygmaeus is an omnivorous, zoophytophagous, generalist predatory mirid with a very wide host range. The application acknowledges that its native species prey list could include 9 whitefly species, 13 aphid species, 19 thrips, up to 46 species of spider mites (some exotic) plus 12 other genera of mites as well as 1582 species of butterflies and . This wide host range, coupled with an ability to invade new environments, are important indicators of a potential pest species. The paucity of research or consideration to our native invertebrates is alarming. There appears to be no studies done to determine the potential for negative impact on these native prey species. There is no information or discussion on the distribution of any of these natives. There is no host testing information. There is no information on the potential for displacement of native Mirid or other insect species through competition. We consider this to be a significantly inadequate assessment.

The application states that “M. pygmaeus will only impact on native populations of host insects where it is able to form self-sustaining populations in habitats supporting native host species”. However, as an inundative or augmented biological control agent with repeated releases of large numbers in greenhouses, the propagule pressure will be considerable, resulting in a high likelihood that M. pygmaeus will escape into the surrounding environment. Thus, there is potential for adverse impact on fauna outside greenhouses, even if M. pygmaeus did not form localised self- sustaining populations. This in turn may lead to impacts in adjacent habitats; and for those particularly threatened invertebrate species there is potential for this to provide the critical tipping point to extinction.

Lepidoptera is specified in the application as having a large number of potential hosts. Like many other New Zealand invertebrate groups Lepidoptera has an extremely high rate of endemism with 90% of the species found only in this

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country (Dugdale 1988). The threat status of many species is of concern as we lack the information to determine their field status. Of the species we do have some understanding of, there are 49 species listed as “Threatened” and a further 69 “At Risk” as well as 56 “Data deficient” species (Hitchmough 2013, Stringer et al., 2012a). Although we have a poor understanding of the factors that influence the threat status of our endemic Lepidoptera, one major factor is thought to be susceptibility to predation by introduced species (Stringer et al., 2012). New introductions of generalist predators such as M. pygmaeus would certainly be an example of this and add to the threat pressures already present.

As well as direct predation to our endemic insect fauna there is the possibility of competitive displacement. This threat is particularly significant for host specific invertebrates such as the 3-4mm long mirid Pimeleocoris viridis. This endemic species is listed as Nationally Critical by Stringer et al., (2102b) and is found only on a single host plant species Pimelea villosa villosa which itself is listed as Declining (de Lange 2009) and is only known from a small area near Kaitaia (Stringer et al., 2012b). The application acknowledges that if M. pygmaeus is capable of establishing anywhere in New Zealand it would be in this area. This could thus pose an extreme risk to the survival of this endemic mirid.

In general we have a very poor understanding of the distribution and ecological interactions of our endemic invertebrate fauna. The above example is one we know of, but there are likely to be many more. Given this paucity of information DOC believes there should be a precautionary approach to any potential introduction of biological agents, particularly those involving generalist predators. We consider the application fails to provide sufficient information to show there will not be significant adverse affect on endemic invertebrates. Native flora

Plant tissue also provides important host material for M. pygmaeus, particularly - but not limited to - solanaceous plants. M. pygmaeus has been found on both Lamiaceae and Geraniaceae species. One study demonstrated that M. pygmaeus can survive solely on eggplant (Solanum melongena) and tomato (Lycopersicon esculentum) in periods of prey scarcity; with its numbers increasing on eggplant in particular (Perdikis and Lykouressis 2004).

The list below shows the many native plants we have in the potentially affected Families and the national status of each. The distribution areas of these species are also indicated to show those that occur within the vulnerable locations as indicated by the CLIMEX modelling. For completeness, the species outside of the vulnerable areas are also listed, and indicated by the gray print.

New Zealand has four native Solanaceae species; 1. Solanum aviculare var. aviculare (declining): NI, SI, multiple sites, including north of Auckland and east coast 2. Solanum aviculare var. latifolium (naturally uncommon): Endemic to northern NI from Coromandel to Three Kings Is. including off-shore islands. Northern Auckland is the NZ stronghold for this variety. 3. Solanum laciniatum (not threatened): NI, SI, multiple sites, including north of Auckland and east coast 4. Solanum nodiflorum (not threatened): multiple sites, north of Auckland and east coast five Lamiaceae species; 5. Mentha cunninghamii (declining): NI, SI Stewart Id, Chatham Is, multiple sites, north of Auckland and east coast 6. Plectranthus parviflorus (coloniser): Northern NI, confined to Whangarei District & Thames-Coromandel District 7. Scutellaria novae-zelandiae (nationally critical) (Nelson and North Marlborough) 8. Teucridium parvifolium (declining):NI and SI, multiple sites, north of Auckland and east coast

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9. Vitex lucens (not threatened): Northern NI to N Taranaki and Gisborne, multiple sites, north of Auckland and east coast, with a NZ stronghold for this species north of Auckland and nine Geraniaceae species: 10. Geranium brevicaule (not threatened) (NI south of Auckland and including east coast, SI and Stewart Island) 11. Geranium homeanum (not threatened): NI, northern SI, multiple sites, north of Auckland and east coast with a NZ stronghold in northern NI 12. Geranium microphyllum (naturally uncommon): endemic to the Auckland and Campbell Islands 13. Geranium potentilloides (not threatened): NI, northern SI, multiple sites although rare in SI, north of Auckland and east coast are both NZ strongholds 14. Geranium retrorsum (nationally vulnerable): multiple sites, north of Auckland and east coast, including many northern offshore islands 15. Geranium sessiliflorum var. arenarium (declining): endemic to South Island, south of Otago Peninsula, Foveaux Strait area and in northern Stewart Island 16. Geranium solanderi (declining): NI and northern SI, multiple sites, including north of Auckland and east coast, and many northern offshore islands 17. Geranium traversii (naturally uncommon): endemic to Chatham Islands, 18. Pelargonium inodorum (not threatened): NI, SI, multiple sites, north of Auckland and east coast with northern NI being a NZ stronghold.

Out of 18 species from potentially affected Families, 15 species occur within the vulnerable areas as indicated by the CLIMEX modelling outcomes. One species has a threat ranking of Nationally Critical, another is Nationally Vulnerable and others have populations in decline. DOC considers M. pygmaeus could be a threat to some or all of these species via either direct plant damage, by vectoring plant diseases or via some other ecosystem function we do not know about. We believe the application fails to adequately assess the level of risk to such hosts if the mirid is released. Conclusions

We consider it inevitable that if introduced into NZ greenhouses M. pygmaeus will escape into the surrounding environment. DOC believes there is insufficient evidence to support the assertion that these escaped M. pygmaeus will not be able to survive outside the greenhouse environment in many areas north of Hamilton and many North Island coastal regions. Due to its extremely wide host range, both in plant and invertebrate species, DOC considers that M. pygmaeus will most certainly find its way to native habitats. Some of these habitats may well contain highly vulnerable native plant and invertebrate species. For those natives that are threatened species with limited distributions, there is potential for significant displacement and adverse impact.

In principle, the Department agrees with De Clercq et al. (2011), who consider the concept of introducing generalist predators and parasitoids for biological control to be an outdated approach, unless the risks can be demonstrated as being very low, because of the potential for extreme risk to non target species. This application fails in that regard and DOC therefore requests that it be declined. References

De Clercq, P., Mason, P. G., Babendreier, D. 2011. Benefits and risks of exotic biological control agents. Biological Control 56(4): 681-698 de Lange P. J., Norton D. A., Courtney, A. P., Heenan, P. B., Barkla, J. W., Cameron, E. K., Hitchmough, R., Townsend, A. J. 2009. Threatened and uncommon plants of New Zealand (2008 revision). New Zealand Journal of Botany 47: 61–96

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Dugdale, J. S. 1988. Lepidoptera – annotated catalogue, and keys to family-group taxa. Fauna of New Zealand 14. DSIR Publishing, Wellington. 264 p.

Hart, A. J.; Tullett, A. G.; Bale, J. S.; Walters, K. F. A. 2002. Effects of temperature on the establishment potential in the UK of the non-native glasshouse biocontrol agent Macrolophus caliginosus. Physiological Entomology. 27(2): 112-123.

Hitchmough, R. A. 2013. Summary of changes to the conservation status of taxa in the 2008-11 New Zealand Threat Classification System listing cycle. New Zealand Threat Classification Series 1. Department of Conservation, Wellington. 20 p.

Perdikis, D. C., and Lykouressis, D. P. 2004. Macrolophus pygmaeus (Hemiptera: Miridae) population parameters and biological characteristics when feeding on eggplant and tomato without prey. Journal of Economic Entomology 97(4):1291-1298. Retrieved January 27, 2014 from http://www.bioone.org/doi/abs/10.1603/0022-0493-97.4.1291.

Stringer, I. A. N., Hitchmough, R. A., Dugdale, J. S., Edwards, E., Hoare, R. J. B., Patrick, B. H. 2012a: The conservation status of New Zealand Lepidoptera, New Zealand Entomologist 35(2): 120-127

Stringer, I. A. N., Hitchmough, R.A., Larivière, M.-C., Eyles, A. C., Teulon, D. A. J.,

Dale, P. J., Henderson, R. C. 2012b: The conservation status of New Zealand Hemiptera, New Zealand Entomologist 35(2): 110-115

Comments co-ordinated on behalf of the Department of Conservation by:

Verity Forbes

Technical Advisor (Biosecurity), Science & Capability

Contributors:

Chris Green, Technical Advisor – Threats (entomology), Science & Capability

Disclosure: Chris Green is a member of the EPA’s Insect Advisory Panel

Shannel Courtney, Senior Ranger Services, Biodiversity (threatened plants), Nelson

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Table 1. Host plant preferences Blank cells = not tested Plant family Plant Nymphal Nymphal Population Reference species development development growth in presence in absence of prey of prey (Ingegno et al. 2011; Asteraceae 10 Calendula officinalis Y N Martinez-Cascales et al. 595 total: 340 native 2006) (Martinez-Cascales et al. Carlina corymbosa 2006) (Lykouressis et al. 2008; Martinez-Cascales et al. Dittrichia viscosa Y N / N Negative11 2006; Maes et al. 2012; Alomar et al. 2002; Parolin et al. 2013) Inula conyza (Perdikis et al. 2000) Brassicaceae Brassica napus Y N (Hatherly et al. 2009) 134 total: 42 native Brassica oleracea Y N (Hatherly et al. 2009) Brassica pekinensis Y N (Hatherly et al. 2009) Cistaceae Cistus spp.12 (Alomar et al. 2002) (Perdikis & Lykouressis Cucurbitaceae Cucumis sativus Y Y / Y Negative13 2003; Perdikis et al. 2000; 10 total: 2 native Alomar et al. 2006) Ecbalium elaterium Y14 (Perdikis et al. 2000) Fabaceae (Martinez-Cascales et al. Phaseolus vulgaris Y 194 total: 36 native 2006; Perdikis et al. 2000) (Martinez-Cascales et al. Ononis natrix 2006) Vicia faba Y (Portillo et al. 2012) Geraniaceae Pelargonium spp. 15 36 total: 9 native Hydrophyllaceae Wigandia (Martinez-Cascales et al.

3 total: 0 native caracasana 2006) Lamiaceae (Martinez-Cascales et al. Ballota hirsuta ? 90 total: 5 native 2006) Salvia officinalis Y N (Ingegno et al. 2011) (Martinez-Cascales et al. Stachys sylvatica Not tested Not tested 2006; HDC 2013) Y – in the (Ingegno et al. 2011; presence of prey Martinez-Cascales et al. Solanaceae (in the absence 2006; Perdikis & Capsicum annuum Y / Y N / Y 71 total: 4 native of prey as the Lykouressis 2004; females did not Perdikis et al. 2000; Maes oviposit_ et al. 2012)

16 Y – in the (Hatherly et al. 2009; Nicotiana tabacum Y N / Y presence of prey Margaritopoulos et al.

10 Total number present in New Zealand: number of those which are natives. 11 Most likely due to the entrapment of the young nymphs on the dense sticky trichomes of D. viscosa in the presence of prey. 12 The original research was conducted in 2002 (Alomar et al. 2002) and later reanalysis showed that the sample was Macrolophus melanotoma (Castañé et al. 2013). Based on this analysis the record is not counted as showing that the plant family is a suitable host for M. pygmaeus. 13 Likely due to honeydew. For example, the insect performed worse when prey were present, which was suspected to be due to honeydew production which can trap or inhibit the smallest nymphal stages from moving freely. Note this effect is very plant and prey specific. 14 When provided with Ecbalium elaterium pollen. 15 Information supplied in the application. We note there are a small number of foreign language publications that we have not been able to access which tentatively support this. 16 This is the standard plant used for rearing M. pygmaeus on.

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Plant family Plant Nymphal Nymphal Population Reference species development development growth in presence in absence of prey of prey 2003) (Ingegno et al. 2011; Solanum Martinez-Cascales et al. Y N / Y lycopersicum 2006; Perdikis et al. 2000; Machtelinckx et al. 2012) Solanum (Martinez-Cascales, 2006) melanogena (Ingegno et al. 2011; Lykouressis et al. 2008; Positive with or Solanum nigrum Y / Y N / Y Martinez-Cascales et al. without prey 2006; Machtelinckx et al. 2012) Solanum tuberosum (Alomar et al. 2002)1 Urticaceae (Martinez-Cascales et al. Parietaria officinalis Y N 16 total: 9 native 2006; Ingegno et al. 2011)

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Table 2. Known hosts (plants and prey) of Macrolophus pygmaeus

Type Species Nymphal development Reference Plants Cucurbitaceae Cucumis sativus Y Table 1 Fabaceae Phaseolus vulgaris Y Table 1 Solanaceae Capsicum annuum Y Table 1 Solanaceae Lycopersicon esculentum Y Table 1 Solanaceae Nicotiana tabacum Y Table 1 Solanaceae Solanum nigrum Y Table 1

Prey

Whitefly 17 (Perdikis et al. 2000; Trialeurodes vaporariorum Y (family Aleyrodidae) Enkegaard et al. 2001) Shown to predate, no Whitefly (Bonato et al. 2006; Alomar Bemisia tabaci studies on development (family Aleyrodidae) et al. 2006) known (Urbaneja et al. 2009; Shown to predate, no Zappalà et al. 2013; Tuta absoluta studies on development (family Gelechiidae) Desneux et al. 2010) known

Moth 18 Spodoptera exigua Y (Tedeschi et al. 1999) (family Noctuidae) Y / Y - including only being raised on this Moth (Castañé & Zapata 2005; Ephestia kuehniella species without access to (family Pyralidae) Vandekerkhove et al. 2011) plant material for 31 generations. Y - Tested only in the Aphid presence of plants, Aphis fabae (non-pest) (Lykouressis et al. 2008) Aphididae accelerated the population growth Y / Y – but negative Aphid (Perdikis & Lykouressis Aphis gossypii population growth rate Aphididae 2003; Perdikis et al. 2000) when on cucumbers Y – but it has only been Aphid Capitophorus inulae tested in the presence of (Lykouressis et al., 2008) Aphididae (non-pest) plant material. Aphid Macrosiphum euphorbiae Y (Perdikis et al. 2000) Aphididae Aphid Only mentioned as Rhopalosiphum padi (Hillert et al. 2002)19 Aphididae predator. Aphid (Perdikis et al. 2000; Myzus persicae Y Aphididae Fantinou et al. 2009) Spider mite (Perdikis et al. 2000; Tetranychus urticae Y Tetranychidae Enkegaard et al. 2001) Y – in lab and in Thrips glasshouse. Not as Frankliniella occidentalis (Blaeser et al. 2004) Thripidae effective control as specialists. Parasitic Wasps Encarsia formosa Not tested (Castañé et al. 2004) Aphelinidae Hoverflies Episyrphus balteatus Eggs – no further testing (Fréchette et al. 2006)20

17 Note T. vaporariorum was the most suitable prey of the five tested for nymphal development, in comparison with the other prey species tested. 18 Based on paper abstract, full text was not able to be accessed. 19 German language paper leaves some uncertainty as to our interpretation; this record should be treated cautiously.

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Type Species Nymphal development Reference Syrphidae Hoverflies Sphaerophoria rueppellii Eggs – no further testing (Fréchette et al. 2006)20 Syrphidae Hoverflies Sphaerophoria scripta Eggs – no further testing (Fréchette et al. 2006)20 Syrphidae Y – in artificial conditions, Mirids 20 Dicyphus tamaninii N – in more realistic (Lucas et al. 2009) Miridae conditions. Could be MM Mirids Recorded but no further Cannibalism (Hamdi et al. 2013) Miridae tested

Artificial diets Artemia franciscana Y – four generations Brine shrimp cysts (Vandekerkhove et al. 2009) Artemia sp. reared Not specifically tested, but plants with extrafloral Extrafloral nectaries NA (Portillo et al. 2012) nectaries available increases survival rate 4x Bee pollen NA Y (Perdikis et al. 2000) N – when cattail pollen is provided as a supplement along with plant material it Cattail pollen NA doubles longevity, but (Portillo et al. 2012) development is not possible on cattail pollen alone (Vandekerkhove & De Egg based diet NA Y Clercq 2010) Y – seventeen generations produced. When given access to Meat based diet NA (Castañé & Zapata 2005) potato sprouts significant improvements in weight, development times etc

20 It is uncertain whether or not this record is of M. pygmaeus or M. melanotoma.

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Table 3. Suggested severity indices for non-target effects of biocontrol agents. From Lynch et al. (2001)

Severity

0  No records of consumption, infection, parasitism, population suppression or extinction

 < 5% mortality induced by consumption/infection/parasitism or equivalent sub-lethal effects on fecundity, with no recorded 1 significant population consequences

2  5–40% mortality from consumption/infection/parasitism, with no recorded significant population consequences

 > 40% mortality from consumption/infection/parasitism (at one time on a local population) and/or significant (> 10%) short-term 3 depression of a local population

4  > 40% short-term depression of a local population, or permanent significant (> 10%) depression of a local population

 > 40% long-term suppression of a local population, or > 10% long-term suppression of a global population (‘global’ meaning an 5 area of 100x100 km or more)

6  > 40% long-term suppression of a global population

7  Apparent local extinction, or extinction where recolonisation likely in the long term

 Certified local extinction where recolonisation is unlikely or impossible (due to an island habitat and/or limited species range, so 8 could imply extinction of the species)

9  Certified extinction over an area of 100x100 km or more

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