Import and release of Macrolophus pygmaeus (Rambur) · Integrated Pest Management by original definition is the integration of biocontrol with chemical applications, so that the latter

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EPA report

Import and release of Macrolophus pygmaeus (Rambur) March 2014

Advice to the Decision Making Committee on application APP201254: – To import and release

Macrolophus pygmaeus as biocontrol agents for whitefly (Trialeurodes vaporariorum), under

section 34 of the Hazardous Substances and New Organisms Act 1996

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

March 2014

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 greenhouse whitefly in tomato 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 insect 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 arthropod 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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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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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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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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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 insects 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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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 animals. 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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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 arthropods, 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

products from the market (Hillocks 2012;

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

Figure 1 Principles of Integrated Pest Management (Reproduced from the U.S. Department of Agriculture)

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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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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, aphids and whiteflies

(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: Hemiptera

Family: Miridae

Tribe: Dicyphini

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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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 [Dicyphus 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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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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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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“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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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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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

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.

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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 animal 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 Macrolophus caliginosus 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 aphid 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 silverleaf whitefly, 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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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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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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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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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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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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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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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 Capsus 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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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

effects and these appear to represent

uncertainty, but we are confident that the

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,

Figure 3 Scientific and technical uncertainty covers a well-defined range of impacts, even where there may appear to be uncertainty on what those effects actually are. The precautionary approach considers the uncertainty of any science outside that range.

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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

sufficient information to indicate that there is a non-

negligible economic benefit to the growers.

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).

Figure 4 Risks to the environment in the immediate vicinity of a glasshouse are negligible, while human health benefits to be gained through reducing OPC applications are likely. Benefits therefore outweigh risks at this scale.

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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

Zealanders in general.

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

to New Zealand, that could act as host

plants for M. pygmaeus. However, we do not

consider that M. pygmaeus will cause any

significant damage to populations of these

plants, and therefore consider this effect to

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.

Figure 5 Risks to the modified environment surrounding glasshouses are non-negligible, and economic benefits are also non-negligible. Benefits are likely to outweigh risks at this scale.

Benefit (unquantified)

Ris

k /

Be

nefit

Risk

Figure 6 Risks to the environment at a regional/national scale are non-negligible, while benefits at this scale are unquantified. Benefits therefore do not outweigh risks in this scenario

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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 Dicyphus hesperus 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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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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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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Figure 7 Slide 1 referred to in comments by Professor Bale


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Appendix 2 Summary of Submitters

Submission Submitter/

organisation

Support/

Oppose

Submitter comments

108116 Nursery and Garden

Industry New Zealand

Support Happy that any concerns Nursery and Garden Industry New

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

Ltd.

Support Growers are struggling with control of whitefly and tomato psyllids in

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

Gardens

Support Reduces reliance on agri-chemicals

Good for the environment, consumers and growers

108119 Karamea Tomatoes

Limited

Support Tomato growers do not have enough products available to control

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

Limited

Support Macrolophus will provide an alternative for controlling whitefly

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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organisation

Support/

Oppose

Submitter comments

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

Council

Concerned There will be benefits from reduced insecticide use

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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organisation

Support/

Oppose

Submitter comments

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

of New Zealand

Oppose No assessment of potential predators already present in New

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

Tomatoes

Support Let us use Macrolophus to manage whitefly

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

Forestry Assn.

Oppose Support biocontrol targeting insect pests

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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organisation

Support/

Oppose

Submitter comments

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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organisation

Support/

Oppose

Submitter comments

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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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

moths. 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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March 2014

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

http://www.bioone.org/doi/abs/10.1603/0022-0493-97.4.1291

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Table 1. Host plant preferences

Blank cells = not tested

Plant family Plant species

Nymphal development in presence of prey

Nymphal development in absence of prey

Population growth

Reference

Asteraceae 595 total: 340 native

10

Calendula officinalis Y N (Ingegno et al. 2011; Martinez-Cascales et al. 2006)

Carlina corymbosa (Martinez-Cascales et al. 2006)

Dittrichia viscosa Y N / N Negative11

(Lykouressis et al. 2008; Martinez-Cascales et al. 2006; Maes et al. 2012; Alomar et al. 2002; Parolin et al. 2013)

Inula conyza (Perdikis et al. 2000)

Brassicaceae 134 total: 42 native

Brassica napus Y N (Hatherly et al. 2009)

Brassica oleracea Y N (Hatherly et al. 2009)

Brassica pekinensis Y N (Hatherly et al. 2009)

Cistaceae Cistus spp.12

(Alomar et al. 2002)

Cucurbitaceae 10 total: 2 native

Cucumis sativus Y Y / Y Negative13

(Perdikis & Lykouressis 2003; Perdikis et al. 2000; Alomar et al. 2006)

Ecbalium elaterium Y14

(Perdikis et al. 2000)

Fabaceae 194 total: 36 native

Phaseolus vulgaris Y (Martinez-Cascales et al. 2006; Perdikis et al. 2000)

Ononis natrix (Martinez-Cascales et al. 2006)

Vicia faba Y (Portillo et al. 2012)

Geraniaceae 36 total: 9 native

Pelargonium spp. 15

Hydrophyllaceae 3 total: 0 native

Wigandia caracasana

(Martinez-Cascales et al. 2006)

Lamiaceae 90 total: 5 native

Ballota hirsuta ? (Martinez-Cascales et al. 2006)

Salvia officinalis Y N (Ingegno et al. 2011)

Stachys sylvatica Not tested Not tested (Martinez-Cascales et al. 2006; HDC 2013)

Solanaceae 71 total: 4 native

Capsicum annuum Y / Y N / Y

Y – in the presence of prey (in the absence of prey as the females did not oviposit_

(Ingegno et al. 2011; Martinez-Cascales et al. 2006; Perdikis & Lykouressis 2004; Perdikis et al. 2000; Maes et al. 2012)

Nicotiana tabacum16

Y N / Y Y – in the presence of prey

(Hatherly et al. 2009; 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 species

Nymphal development in presence of prey

Nymphal development in absence of prey

Population growth

Reference

2003)

Solanum lycopersicum

Y N / Y

(Ingegno et al. 2011; Martinez-Cascales et al. 2006; Perdikis et al. 2000; Machtelinckx et al. 2012)

Solanum melanogena

(Martinez-Cascales, 2006)

Solanum nigrum Y / Y N / Y Positive with or without prey

(Ingegno et al. 2011; Lykouressis et al. 2008; Martinez-Cascales et al. 2006; Machtelinckx et al. 2012)

Solanum tuberosum (Alomar et al. 2002)1

Urticaceae 16 total: 9 native

Parietaria officinalis Y N (Martinez-Cascales et al. 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 (family Aleyrodidae)

Trialeurodes vaporariorum17

Y (Perdikis et al. 2000; Enkegaard et al. 2001)

Whitefly (family Aleyrodidae)

Bemisia tabaci Shown to predate, no studies on development known

(Bonato et al. 2006; Alomar et al. 2006)

Moth (family Gelechiidae)

Tuta absoluta Shown to predate, no studies on development known

(Urbaneja et al. 2009; Zappalà et al. 2013; Desneux et al. 2010)

Moth (family Noctuidae)

Spodoptera exigua Y (Tedeschi et al. 1999)18

Moth (family Pyralidae)

Ephestia kuehniella

Y / Y - including only being raised on this species without access to plant material for 31 generations.

(Castañé & Zapata 2005; Vandekerkhove et al. 2011)

Aphid Aphididae

Aphis fabae (non-pest)

Y - Tested only in the presence of plants, accelerated the population growth

(Lykouressis et al. 2008)

Aphid Aphididae

Aphis gossypii Y / Y – but negative population growth rate when on cucumbers

(Perdikis & Lykouressis 2003; Perdikis et al. 2000)

Aphid Aphididae

Capitophorus inulae (non-pest)

Y – but it has only been tested in the presence of plant material.

(Lykouressis et al., 2008)

Aphid Aphididae

Macrosiphum euphorbiae Y (Perdikis et al. 2000)

Aphid Aphididae

Rhopalosiphum padi Only mentioned as predator.

(Hillert et al. 2002)19

Aphid Aphididae

Myzus persicae Y (Perdikis et al. 2000; Fantinou et al. 2009)

Spider mite Tetranychidae

Tetranychus urticae Y (Perdikis et al. 2000; Enkegaard et al. 2001)

Thrips Thripidae

Frankliniella occidentalis

Y – in lab and in glasshouse. Not as effective control as specialists.

(Blaeser et al. 2004)

Parasitic Wasps Aphelinidae

Encarsia formosa Not tested (Castañé et al. 2004)

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 Syrphidae

Sphaerophoria rueppellii Eggs – no further testing (Fréchette et al. 2006)20

Hoverflies Syrphidae

Sphaerophoria scripta Eggs – no further testing (Fréchette et al. 2006)20

Mirids Miridae

Dicyphus tamaninii Y – in artificial conditions, N – in more realistic conditions. Could be MM

(Lucas et al. 2009)20

Mirids Miridae

Cannibalism Recorded but no further tested

(Hamdi et al. 2013)

Artificial diets

Brine shrimp cysts Artemia franciscana Artemia sp.

Y – four generations reared

(Vandekerkhove et al. 2009)

Extrafloral nectaries NA

Not specifically tested, but plants with extrafloral nectaries available increases survival rate 4x

(Portillo et al. 2012)

Bee pollen NA Y (Perdikis et al. 2000)

Cattail pollen NA

N – when cattail pollen is provided as a supplement along with plant material it doubles longevity, but development is not possible on cattail pollen alone

(Portillo et al. 2012)

Egg based diet NA Y (Vandekerkhove & De Clercq 2010)

Meat based diet NA

Y – seventeen generations produced. When given access to potato sprouts significant improvements in weight, development times etc

(Castañé & Zapata 2005)

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

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

significant population consequences

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

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

depression of a local population

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

5 > 40% long-term suppression of a local population, or > 10% long-term suppression of a global population (‘global’ meaning an

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

8 Certified local extinction where recolonisation is unlikely or impossible (due to an island habitat and/or limited species range, so

could imply extinction of the species)

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

64

EPA advice APP201710

. March 2014

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Alomar, Ò., Riudavets, J. & Castañe, C., 2006. Macrolophus caliginosus in the biological control of Bemisia tabaci on greenhouse melons. Biological Control, 36(2), pp.154–162. Available at: http://linkinghub.elsevier.com/retrieve/pii/S104996440500232X [Accessed January 5, 2014].

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Bale, J., 2011. Harmonization of regulations for invertebrate biocontrol agents in Europe: progress, problems and solutions. Journal of Applied Entomology, 135(7), pp.503–513. Available at: http://doi.wiley.com/10.1111/j.1439-0418.2011.01611.x [Accessed February 2, 2014].

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Battaglia, D. et al., 2013. Tomato belowground-aboveground interactions: Trichoderma longibrachiatum affects the performance of Macrosiphum euphorbiae and its natural antagonists. Molecular Plant-Microbe Interactions, 26(10), pp.1249–1256. Available at: http://apsjournals.apsnet.org/doi/abs/10.1094/MPMI-02-13-0059-R [Accessed January 19, 2014].

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Hamdi, F. et al., 2013. Evidence of Cannibalism in Macrolophus pygmaeus, a Natural Enemy of Whiteflies. Journal of Insect Behavior, 26(4), pp.614–621. Available at: http://link.springer.com/10.1007/s10905-013-9379-3 [Accessed December 24, 2013].

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Hatherly, I.S., Pedersen, B.P. & 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(1), pp.35–45. Available at: http://link.springer.com/10.1007/s10526-008-9155-z [Accessed December 24, 2013].

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