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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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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
Figure 8 Slide 2 referred to in comments by Professor Bale
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Figure 9 Slide 3 referred to in comments by Professor Bale
Figure 10 Slide 4 referred to in comments by Professor Bale
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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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Submission Submitter/
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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Submission Submitter/
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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Submission Submitter/
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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Submission Submitter/
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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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
58
Application for approval to import and release Macrolophus pygmaeus (APP201254)
March 2014
Dugdale, J. S. 1988. Lepidoptera – annotated catalogue, and keys to family-group taxa. Fauna of New Zealand 14. DSIR
Publishing, Wellington. 264 p.
Hart, A. J.; Tullett, A. G.; Bale, J. S.; Walters, K. F. A. 2002. Effects of temperature on the establishment potential in the
UK of the non-native glasshouse biocontrol agent Macrolophus caliginosus. Physiological Entomology. 27(2): 112-123.
Hitchmough, R. A. 2013. Summary of changes to the conservation status of taxa in the 2008-11 New Zealand Threat
Classification System listing cycle. New Zealand Threat Classification Series 1. Department of Conservation,
Wellington. 20 p.
Perdikis, D. C., and Lykouressis, D. P. 2004. Macrolophus pygmaeus (Hemiptera: Miridae) population parameters and
biological characteristics when feeding on eggplant and tomato without prey. Journal of Economic Entomology
97(4):1291-1298. Retrieved January 27, 2014 from http://www.bioone.org/doi/abs/10.1603/0022-0493-97.4.1291.
Stringer, I. A. N., Hitchmough, R. A., Dugdale, J. S., Edwards, E., Hoare, R. J. B., Patrick, B. H. 2012a: The conservation
status of New Zealand Lepidoptera, New Zealand Entomologist 35(2): 120-127
Stringer, I. A. N., Hitchmough, R.A., Larivière, M.-C., Eyles, A. C., Teulon, D. A. J.,
Dale, P. J., Henderson, R. C. 2012b: The conservation status of New Zealand Hemiptera, New Zealand Entomologist
35(2): 110-115
Comments co-ordinated on behalf of the Department of Conservation by:
Verity Forbes
Technical Advisor (Biosecurity), Science & Capability
Contributors:
Chris Green, Technical Advisor – Threats (entomology), Science & Capability
Disclosure: Chris Green is a member of the EPA’s Insect Advisory Panel
Shannel Courtney, Senior Ranger Services, Biodiversity (threatened plants), Nelson
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Table 1. Host plant preferences
Blank cells = not tested
Plant family Plant 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
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References
Alomar, Ò., Goula, M. & Albajes, R., 2002. Colonisation of tomato fields by predatory mirid bugs (Hemiptera: Heteroptera) in northern Spain. Agriculture, Ecosystems & Environment, 89(1-2), pp.105–115. Available at: http://linkinghub.elsevier.com/retrieve/pii/S016788090100322X.
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].
Arnó, J. & Gabarra, R., 2011. Side effects of selected insecticides on the Tuta absoluta (Lepidoptera: Gelechiidae) predators Macrolophus pygmaeus and Nesidiocoris tenuis (Hemiptera: Miridae). Journal of Pest Science, 84(4), pp.513–520. Available at: http://link.springer.com/10.1007/s10340-011-0384-z [Accessed December 12, 2013].
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].
Barratt, B.I.P. et al., 1997. Laboratory Nontarget Host Range of the Introduced Parasitoids Microctonus aethiopoides and M . hyperodae (Hymenoptera : Braconidae) Compared with Field Parasitism in New Zealand. Biological Control, 26, pp.694–702.
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].
Beggs, J., 2001. The ecological consequences of social wasps (Vespula spp.) invading an ecosystem that has an abundant carbohydrate resource. Biological Conservation, 99(1), pp.17–28. Available at: http://linkinghub.elsevier.com/retrieve/pii/S0006320700001853.
Bioforce, 2014. Enforce TM
for Greenhouse Whitefly Control. , pp.1–4. Available at: http://www.bioforce.net.nz/site/bioforce/files/PDFs/Enforce.pdf [Accessed January 9, 2014].
Blaeser, P., Sengonca, C. & Zegula, T., 2004. The potential use of different predatory bug species in the biological control of Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). Journal of Pest Science, 77(4), pp.211–219. Available at: http://link.springer.com/10.1007/s10340-004-0057-2 [Accessed December 12, 2013].
Bonato, O., Couton, L. & Fargues, J., 2006. Feeding Preference of Macrolophus caliginosus ( Heteroptera : Miridae ) on Bemisia tabaci and Trialeurodes vaporariorum ( Homoptera : Aleyrodidae ) Feeding Preference of Macrolophus caliginosus ( Heteroptera : Miridae ) on Bemisia tabaci and Trialeurodes. Journal of Economic Entomology, 99(4), pp.1143–1151.
Bonato, O. & Ridray, G., 2007. Effect of tomato deleafing on mirids, the natural predators of whiteflies. Agronomy for sustainable development, 27, pp.167–170. Available at: http://link.springer.com/article/10.1051/agro:2007011 [Accessed January 5, 2014].
Buckley, T.R. & Bradler, S., 2010. Tepakiphasma ngatikuri , a new genus and species of stick insect (Phasmatodea) from the Far North of New Zealand. New Zealand Entomologist, 33(1), pp.118–126. Available at: http://www.tandfonline.com/doi/abs/10.1080/00779962.2010.9722200 [Accessed January 22, 2014].
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Castañé, C. et al., 2004. Colonization of tomato greenhouses by the predatory mirid bugs Macrolophus caliginosus and Dicyphus tamaninii. Biological Control, 30(3), pp.591–597. Available at: http://linkinghub.elsevier.com/retrieve/pii/S1049964404000325 [Accessed December 21, 2013].
Castañé, C. et al., 2011. Plant damage to vegetable crops by zoophytophagous mirid predators. Biological Control, 59(1), pp.22–29. Available at: http://linkinghub.elsevier.com/retrieve/pii/S104996441100065X [Accessed December 12, 2013].
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