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Background information on biological control safety

Biological control

Biological control is usually defined as the use of natural enemies to suppress populations of pests such as insects and weeds. In new areas or countries, pests often arrive without the suite of natural enemies which would normally keep then in check in their natural range. Consequently they sometimes undergo periods of outbreak before existing predators, parasitoids or diseases adapt to them, and before pest management strategies, including biological control can be developed.

Biological control has a long history dating back to 200 A.D. when the Chinese used natural enemies to control insect pests. Ants were used (and nests of ants sold) to control citrus insect pests, and ants were also used in 1200 A.D. in Yemen for control of date palm pests by moving nests from the wild and placing them in the trees. At about the same time ladybird beetles were recognised as being useful for control of aphids and scale insects. For more on the history of biological control see Simmonds et al. (1976). In New Zealand the earliest biological control agent introduction was Coccinella undecimpunctata, a coccinellid predator released in 1874 to attack aphids (Cameron et al. 1993).

Biological control can be used for pest management in a number of ways:

Natural enemies

There are several basic texts on biological control which give background information on different types of biological control, biological control agents and successes of biological control (e.g. (van den Bosch et al. 1982, DeBach and Rosen 1991, van Driesche and Bellows 1996).

Natural enemies of invertebrate pests

Natural enemies of weeds

Phytophagous insects and mites have been used extensively for weed biological control, but plant pathogens have also been used. Weed biological control agents can target seeds, foliage, stems or roots of the weed, and combinations of agents attacking different parts of the plant are often employed. Biological control can reduce plant vigour so that other controls are more effective in integrated weed management systems.

Environmental risks of biological control

The environmental risk of pesticide use was forcefully publicised by Rachel Carson in her book Silent Spring (Carson 1963). This landmark publication signalled a turning point, particularly in the USA, when public pressure to reduce the amount of pesticides used on crops, as well as the development of increasing levels of pesticide resistance, and promotion of the philosophy of sustainable agricultural practices, resulted in public outcry and the demand for alternatives to pesticides. Biological control became one of the obvious choices and Ehler (1990) quoted some of the world's most prestigious biological control researchers, who gave the following assurances about the safety of biological control:
"...no adverse effects on the ecosystem occur from biological control" (DeBach 1974);
"...research in this sphere [biological control] results in prodigious economic benefits - without any environmental hazards..." (Simmonds and Bennett 1977);
"The use of predators and parasites for pest control, when it is the result of a well thought out, carefully executed program, is in our opinion, risk-free" (Caltagirone and Huffaker 1980).

However, when considering biological and chemical control methods, it is clear that in comparison with the latter, biological control is irreversible, self-perpetuating and self-dispersing. These attributes are, of course, amongst the benefits of biological control as a component of sustainable pest management programmes, but they are also the factors which have alerted researchers to the potential environmental implications of such introductions.

Assurances regarding the environmental safety of biological control were questioned (e.g. (Howarth 1983, Howarth 1991, Samways 1994, Simberloff and Stiling 1996), and for a few years views became highly polarised, particularly in the USA. Biological control practitioners became very defensive, claiming that the 'conservationists' had no evidence for negative impacts of biological control (e.g. (Howarth and Ramsay 1991, Hopper 1995, Strand and Obrycki 1996 pointed out that the lack of evidence for negative environmental impacts of biological control introductions is a result more of the lack of study of effects than the absence of these impacts. Lockwood (1993) argued that the pitfalls of biological control were the non-target effects, possibly leading to species extinction, the high failure rate of biological control programmes and the inability to explain failure. He attributed some of these consequences to the lack of adequate legislative requirements for quarantine and post-release studies for biological control agents for insect pests. In recent years, however, more funding has become available for research into non-target impacts of biological control, and researchers have taken the opportunity to conduct good ecological research in this area to the benefit of environmentally safer biological control.

Safe use of biological control can lead to enormous economic and environmental benefits and regulation must take into account the risk of rejecting potentially useful species by over-cautious decisions.

Direct effects

Adding a new species to an ecosystem is bound to impact in some way. The complex nature of communities precludes prediction of the ramifications that might occur through the trophic levels within the system. The potential risks from biological control introductions come from either direct effects on non-target species or indirect effects on the community into which the new species arrives. Novel hosts might include indigenous species that are taxonomically related to the intended host including beneficial or valued species, and species which occur in or near the habitats where the target host is found, or to where it disperses.

Until recently, there has been little research undertaken to demonstrate the impact of biological control agents on populations of non-target species. It has been shown that the weevil Rhinocyllus conicus (Froehlich), introduced into the USA to control exotic thistles, has also adopted native thistle species as hosts and impacts at the population level have been demonstrated (Louda 1999, Louda et al. 2005). This is one of few examples where the impact of a biological control agent on non-target species has been quantified. In New Zealand, the braconid parasitoid Microctonus aethiopoides Loan, introduced to control the weevil lucerne pest Sitona discoideus Gyllenhal, has been found to parasitise a number of non-target weevil species in the field, with parasitism levels of up to 70% (Barratt et al. 1997). Ironically, one of the species attacked by M. aethiopoides in New Zealand is the weed biological control agent, R. conicus (Ferguson et al. 1998), although the impact of this on thistle control has not been assessed.

The most well documented examples of adverse impacts from biological control programmes have involved the introduction of vertebrates. The Indian mongoose (Herpestes auropunctatus) was introduced to the West Indies and Hawaii to control rats in sugarcane, but being unable to climb trees, it was only able to control the Norway rat and not the less numerous tree rat. The latter, having been suppressed by the former, then became more abundant. The mongoose also attacked domestic and native birds and lizards, and the reduction in numbers of lizards resulted in an increase in numbers of the sugarcane beetle (Pimentel 1980). The other classical example is the introduction of the cane toad (Bufo marinus) from Central and South America in to Queensland to control two pests of sugar cane, the grey backed cane beetle and French's beetle. While biological control of the sugar cane pests failed, the toad has spread spectacularly within Australia and reached very high population densities and posed a threat to native species in some areas.

There are examples also of generalist predators which have been very damaging to non-target organisms, for example the predatory snail, Euglandina rosea. This was released in many countries, often contrary to the advice of scientists, to control the giant African snail, Achatina fulica, a pest of crops and natural ecosystems. However, E. rosea has had a devastating effect on native snails, in some instances causing extinctions (Civeyrel and Simberloff 1996).

Given the regulatory safeguards that we have in place today, such poorly conceived deliberate introductions are unlikely. However, impacts of invertebrates are less obvious and hence more difficult to investigate. Consequently there are few well documented cases of adverse impacts of biological control agents. There is circumstantial evidence to suggest that insect biological control agents have the capacity to cause species extinctions, particularly in island communities. In Fiji, the introduction of the tachinid Bessa remota (Aldrich) to control the coconut moth, Levuana iridescens Bethune-Baker is reported to have caused the extinction of its host (Howarth 1991). Similarly, the citrus psylla, Trioza erytreae (Del Guericio) was apparently exterminated from Reunion Island by the eulophid parasitoid Tetrastichus dryi Waterston (Aubert and Quilici 1983). In both cases, the parasitoids maintained their populations on alternative species, despite the decline of the target hosts. Whether or not L. iridescens is actually extinct is still hotly debated.

Indirect effects

Non-target impacts can be very complex and unpredictable. A good example of this is the extinction of the large blue butterfly, Maculinea arion (L.) partly attributable to the biological control of rabbits in the UK using the myxoma virus (Wells et al. 1983). The butterfly larvae live in ants nests and feed on the brood of Myrrmica ants. Changing land use coupled with the rapid decline of rabbits in the UK caused many grassland habitats to revert to scrub with loss of suitable habitat for the ants. In New Zealand, the introduced braconid wasp, M. aethiopoides attacks several non-target weevil species including native broad-nosed weevils (Barratt et al. 2000). In native grassland sown with legumes to improve soil fertility, these weevils can cause severe damage to the developing legume seedlings. While parasitism by M. aethiopoides could be considered an added benefit, the native weevils are also weed seedling feeders and may play a role in controlling the seedling establishment of Hieracium (hawkweed), a serious agricultural and conservation weed in native grassland (Evans et al. 1994).

Biological control of weeds is generally assessed to be low risk if they do not directly attack non-target species, however, by evaluation of case studies Pearson and Callaway (2005) found that indirect effects can be demonstrated in some cases. They found that while difficult to predict, indirect non-target effects of host specific biological control agents were proportional to the biological control agents abundance, which was higher for moderately successful agents than those which were highly successful. They concluded that the most low-risk biological control agents are both highly effective, and host specific. Holt and Hochberg (2001) similarly concluded from their theoretical models that a biological control agent which is only moderately effective in controlling abundance of the target may be more abundant, and hence pose a greater risk to non-target species than a highly effective biological control agent. Clearly a case-by case analysis of risk is essential.

Another approach to investigating indirect effects of biological control agents has been the construction of food webs. Willis and Memmott (2005) used a weed biological control example to show that food webs can be used to demonstrate indirect effects of biological control agents. In the particular case discussed, the biological control agent served to increase the abundance, and change the community structure, of native parasitoids.

Another example, described in detail by Barratt et al. (2006) of unexpected indirect effects comes from weed biological control. A number of biological control agents were introduced into North America for Centaurea maculosa Lamarck (spotted knapweed) control. Two tephritid flies, Urophora quadrifasciata (Meigen) and Urophora affinis Frauenfeld became widespread and abundant, and the larvae overwinter in the galled flower heads until they pupate and emerge in the spring. This food resource has attracted the deer mouse, Peromyscus maniculatus which can consume several hundred Urophora larvae/day constituting >80% of its diet. Mouse populations have increased up to 3-fold and over-winter mortality of mice is greatly reduced in the presence of knapweed. However, a major concern raised by this indirect effect on deer mice is that they are the main carrier of Sin Nombre hantavirus, which can cause significant human mortality.

Reducing the risk

It must be accepted that the risk of adverse impacts from biological control releases can probably never be eliminated. However, carefully conceived containment or quarantine studies can almost certainly reduce risk. Protocols for host specificity testing of weed biological control agents have been developed which depend upon a system of 'centrifugal phylogenetic testing' (Wapshere 1974). This means that non-target species from those most closely related to the target weed to those more distantly related are exposed in sequence to the proposed biological control agent. This enables a profile of the host range of the organism to be developed and facilitates the decision on whether or not to proceed with field release. With insects, assembling a suitable list of potential non-target species to be tested is more difficult because of the much larger number of species involved, and the lack of precise taxonomic information. However, the principles of the system used for weed biological control agents can to some extent be extended to insects.

There has been considerable debate about the desirability of host specificity in proposed biological control agents. While some contend that the presence of alternative hosts can assist the biological control agent through periods when the target host is scarce (Nechols et al. 1992), others maintain that it is irresponsible to release any biological control agent unless it can be demonstrated to be completely host specific. Then again, it is argued that laboratory tests can be unreliable because in confinement in an artificial environment, some proposed biological control agents attack species that would not be attacked in the field (Sands 1993) and vice versa. There is still a great deal of research that needs to be carried out to underpin the design of reliable and feasible protocols. A possible approach is to verify the pre-release predictions of host range made from laboratory tests with post-release field studies to determine realised host range in the field (Barratt et al. 1997). This can help to build up a database which can assist decision makers in the future. Clearly, the environmental risks associated with the introduction of a biological control agent have to be weighed against the economic benefits of controlling a pest, or in some cases, the environmental cost of doing nothing.

Biological control best practice

In many countries, regulation of biological control agent introduction has been tightened in recent years. In 1995, the FAO Council ratified an international 'Code of Conduct for the Import and Release of Biological Control Agents' with the intention of providing a set of standards and guidelines for 'best practice' biological control agent introduction (Schulten 1997), and this has recently been updated (Nowell and Maynard 2005). It is recommended in the Code that proposed importers of biological control agents provide information on agricultural and environmental non-target effects. It is accepted that regulation of biological control agent introduction is required in the public interest because of its irreversibility, and the potential for biological control agents to disperse to habitats other than those where they were released (van Lenteren 1997). In New Zealand, the HSNO Act 1996 requires that new organism introductions, including biological control agents must be compatible with safeguarding the life-supporting capacity of air, water and ecosystems, the sustainability of flora and fauna, and the intrinsic value of ecosystems (ERMA New Zealand 1998).

Selecting suitable targets for biological control

Much thought goes into selecting suitable biological control agents but it is initially important to ensure that the target is a suitable candidate for biological control. Sheppard (1992) pointed out that while success of weed biological control agents is only about 35%, if the analysis is based on the target weed rather than the agent, success can be as high as 65%. Fowler (2000) calculated that when funding and support is adequate, success rate for weed biocontrol is about 50-80%.

Charudattan (2005) discussed the factors involved in selecting a good biological control target for pathogens used for inoculative and inundative augmentative biological control. The author concluded that a target weed needs to have strong stakeholder interest, that there is a good candidate pathogen, and that biocontrol with the candidate pathogen will be as cost effective as other control options. It was also pointed out that weeds with good vegetative regeneration capacity, and species with genetic heterogeneity are more difficult to control with pathogens, but that annual, perennial and biennial weeds are equally good targets.

Although the EPA is concerned mainly with avoiding the release of new organisms that might be detrimental to natural ecosystems, to human health and well-being etc., they also have regard for the economic or environmental justification for the release. Since there is always a degree of uncertainty about environmental impacts, it is not worth taking that risk if the benefits are not shown to be potentially worthwhile.

For more detailed information on this topic see the section on Selecting Biological Control Agents.

Biological control agent selection

Selection of appropriate biological control agents is obviously critical to any biological control programme, and justification of this selection will be expected by the EPA in the application. Some of the factors that will be considered, and the type of information that should be provided, are discussed below.

Biological control agent selection usually follows a detailed investigation or 'exploration' in the country of origin of the target pest. Here natural enemies are observed, collected, and ideally tested for host range. These studies are likely to be essential in assessing efficacy of the biological control agent in relation to the target, but might also signal the likely breadth of host range.

Increasing emphasis on target and potential non-target effects is putting pressure on biological control practitioners to improve the selection methods for biological control agents, with one of the aims being to reduce the number required to achieve successful control. An effective agent has to establish in the new country, and reach and maintain a sufficient population size to cause significant damage to critical stages of the target pest's life cycle. Knowledge of the ecology of the target host, whether it is a weed or insect pest, and of the potential agents can help in the selection of the most effective agents.

The degree of host specificity is clearly very important for environmental safety determination, so characteristics of biological control agents that have a bearing on host specificity are worth examining. Table 1 categorizes some features of predators and parasitoids that might affect host specificity. A parasitoid is likely to have a narrower host range than a predator because its more intimate relationship with its host generally demands greater specialization. Similarly, an endoparasitoid has to adapt to the physiology of its host, thus requiring additional specialization and further limiting host range. For the same reason, koinobionts generally have a narrower host range than idiobionts (Askew and Shaw 1986). Linked with this is the mechanism by which the host immune response is overcome. This often requires the injection of venom or other parasitoid-derived proteins during oviposition, but some braconids and ichneumonids deliver polydnavirus or other virus-like particles (Vinson 1990), some of which transcribe proteins in the host to bring about host immunosuppression (Webb and Summers 1990). Since the symbiont is a genetically variable organism with the potential to modify host physiology (Stoltz and Xu 1990), this could provide a mechanism for host range expansion (Whitfield 1994). Interestingly, M. aethiopoides, which attacks several non-target weevils in New Zealand, has virus-like particles (VLPs) which are structurally similar to polydnavirus (Barratt et al. 1999), but no VLPs have been found in M. hyperodae, which has a very narrow host range (Barratt et al. 2006).

Host characteristics that influence host range should also be considered. For example, a mobile, dispersive host with a broad plant host range could transport or attract a parasitoid into contact with a greater diversity of potential non-target hosts than a sedentary host restricted to a specific crop plant, or a plant with a limited distribution. It has been suggested there is more environmental constancy in late succession plants and therefore more opportunity for specialization by parasitoids attacking herbivores of late successional plants (Godfray 1994). There are undoubtedly other characteristics that could be added to this list, but this type of information alone cannot be regarded as a guide to the suitability of biological control agents. Hawkins and Marino (1997) analysed a number of variables which might help explain parasitoid host range expansion in North America, including some of those in Table 1, and found very little correlation. They concluded that either their data were inadequate, or that the processes determining host range are extremely complex and unpredictable.

Table 1. Characteristics of parasitoids believed to be associated with either polyphagy or oligophagy.
More polyphagousMore oligophagous
PredatorParasitoid
EctoparasitoidEndoparasitoid
IdiobiontKoinobiont
Host immuno-suppression by symbionts e.g. polydnavirusHost immunosuppression by non-symbionts
Mobile, dispersive hostSedentary host
Host generalist feeder or on widely distributed plantsHost crop-specific or restricted to plants with limited distribution
Host on early successional plantsHosts on late successional plants

For pathogens, Knudsen et al. (1997) have provided a useful review of the types of screening protocols available, but they stress importance of a good understanding of the life cycle of the pest organism, particularly inoculum transfer and critical inoculum threshold levels under field conditions rather than depending upon laboratory methods.

Host specificity characteristics of weed biological control agents is discussed in the section on containment testing.

Host life stage attacked

The stage of the life cycle of the target host that is attacked by a potential biological control agent is clearly important in terms of efficacy, and impact on population density. In terms of biosafety it is also potentially significant. For example, a parasitoid of a sedentary stage of the life cycle might pose less of a risk to non-target hosts than one which attacks a dispersive phase of the life cycle. Biological control agents of weeds might target the foliage, reproductive structures, stems, crown, roots etc. and the impact of the biological control agent will be dependent upon the ability of the plant to recover and/or compensate for damage. When combinations of biological control agents are used, the approach taken is often to target different parts of the plant. The possibility of one biological control agent compromising the impact of another is clearly best avoided as noted below.

Possible interactions with existing biological control agents for the target host

When considering the introduction of a new biological control agent, it is important to be aware of existing biological control agents (see BCANZ [http://b3.net.nz/bcanz/]) whether they have been deliberately released in the past or arrived accidentally, or indeed if they are naturally occurring. This is something that is usually addressed by the EPA (and ERMA NZ before them) and taken into consideration when making a decision. When applying for a biological control release, it is advisable to take into account existing natural enemies and attempting to predict as far as possible what interactions are likely to occur. For example, in the case of the application to introduce the gall fly, Procecidochares alani to control mist flower, complementarity between this proposed biological control agent and the previously introduced fungus Entyloma ageratinae was considered to be a key issue. The following is taken from the decision [http://www.epa.govt.nz/search-databases/HSNO%20Application%20Register%20Documents/NOR99004.doc] published by ERMA New Zealand, and can be found on the EPA website:

"The Committee was concerned that the benefits of introducing P. alani over and above those provided by the existing mist flower biological control agent, E. ageratinae, were not clear. The Committee therefore considered a key issue to be the extent of complementarity between the two control agents.

It is noted that the degree of control likely to be achieved by a biological control agent is largely unpredictable and is a function of the particular biological control agent-host-environment combination. Evidence recorded to date in New Zealand suggests that the impact of E. ageratinae is likely to be uneven geographically, seasonally and from year to year. In particular, the requirement of the fungus for moisture to successfully infect leaves, means that E. ageratinae will probably be most active at wet periods of the year and least active in mid-summer. The optimum temperature for E. ageratinae is several degrees lower than P. alani, also suggesting the fungus would be more active than P. alani in spring and autumn.

P. alani is likely to be most abundant and damaging in mid to late summer, coinciding with peak abundance of mist flower growing points into which flies can deposit eggs. Field observations in Hawaii and laboratory evidence suggest that P. alani can suppress the growth of mist flower in the absence of E. ageratinae. But were both agents to occur at the same site, it is possible that the production of galls during summer by P. alani may have an additive impact on mist flower, if plants were already stressed from defoliation by fungal attack during spring. The Committee notes that research to measure the relative impacts of these agents and their interactions has not been undertaken in Hawaii, and would have to await release of both agents into New Zealand.

Based on their habitat preferences, life cycles and modes of attack, it appears likely that P. alani and E. ageratinae will work in a complimentary fashion. It is also likely that some sites will be more conducive to one agent than the other, depending on environmental conditions such as moisture, temperature and exposure to wind and sun. Therefore, release of P. alani may increase the number of sites where mist flower is subject to biological control. The Committee concludes that if P. alani establishes, it is likely to provide additional benefits over and above those of the existing biological control programme against mist flower."

This extract from the decision on mist flower is reproduced in full to illustrate the degree of detail that was required at the time by ERMA New Zealand to assess complementarity between existing and proposed biological control agents. Clearly it is not in the interests of NZ to introduce a new organism which is likely to jeopardise the activity of an existing natural enemy, and hence the EPA would have to consider this as a potential risk factor.

Guide to key elements of the Hazardous Substances and New Organisms (HSNO) Act 1996

Introduction to the HSNO Act

Introduction of any new organisms into New Zealand is regulated under the HSNO Act [http://www.legislation.govt.nz/act/public/1996/0030/latest/DLM381222.html]. The legislation is strongly focussed on the health and safety of people and the environment. HSNO provides a framework for assessment and approval of applications to import, develop, field test, conditionally release or release novel compounds, microorganisms, plants, and animals that are new organisms including genetically modified organisms (GMOs). Clearly, biological control agents are subject to the HSNO Act.

The purpose of the HSNO Act

The purpose of the Act is to protect the environment, and the health and safety of people and communities, by preventing or managing the adverse effects of hazardous substances and new organisms. Principles to be recognized and provided for in the legislation include safeguarding the life-supporting capacity of air, water, soil, and ecosystems. There are matters to be taken into account in relation to the purpose of the Act, which include the sustainability of all native and valued introduced flora and fauna, intrinsic value of ecosystems, public health, relationship of the Maori people with the biophysical state, economic and related benefits and costs, and New Zealand's international obligations. The Authority is required to take into account the need for caution in managing adverse effects, where there is scientific and technical uncertainty about those effects. The HSNO Act is implemented by the EPA, (formerly the Environmental Risk Management Authority), a quasi-judicial body of 6�8 people appointed by the Minister for the Environment who are selected to represent a 'balanced mix of knowledge and experience' in the appropriate areas. The Authority is supported by the staff and infrastructure of the government Agency and together the Authority and the Agency form the EPA (the Environmental Protection Authority). While assessing effects, the decision-making Authority is required to use a consistent methodology that was developed as a regulation in 1998 (ERMA New Zealand 1998).

The Methodology

The HSNO Act specified that a 'methodology' for processing applications was to be developed. ERMA New Zealand prepared a draft methodology, which was subject to public submissions before finalising the document (ERMA New Zealand 1998). The Methodology [http://www.epa.govt.nz/Publications/Annotated-Methodology.pdf] can be found on the EPA website. This document explains the nature of the information that applicants are responsible for supplying to the EPA:

"In making applications, applicants will be responsible for:

The 'methodology' also gives requirements for submitters:

"People making submissions on publicly notified applications have a responsibility to:

Also contained within The Methodology [http://www.epa.govt.nz/Publications/Annotated-Methodology.pdf] is an explanation of the decision paths that will be used by the Authority, information on Maori perspectives, the approach to risk, cost and benefit identification and assessment, and how the Authority will deal with uncertainty:

"29. Where the Authority encounters scientific and technical uncertainty relating to the potential adverse effects of a substance or organism, or where there is disputed scientific or technical information the Authority �
(a) Must determine the materiality and significance to the application of the uncertainty or dispute taking into account the extent of agreement on the scope and meaning of the scientific evidence; and
(b) May, where the uncertainty or dispute is material or significant, facilitate discussion between the parties concerned to clarify the uncertainty or dispute.

30. Where any scientific or technical uncertainty or dispute is not resolved to the Authority's satisfaction during its consideration of the application, the Authority must take into account the need for caution in managing the adverse effects of the substance or (to the extent provided for under the Act) the organism concerned.

31. Where the Authority considers that uncertainty arises from an absence of information, or inconclusive or contradictory information, or information from an unreliable source, the Authority may request the applicant to provide further information in accordance with section 58 of the Act and must take full account of any additional information provided.

32. Where the Authority considers there is uncertainty in relation to costs, benefits, and risks (including, where applicable, the scope for managing those risks), the Authority must attempt to establish the range of uncertainty and must take into account the probability of the costs, benefits, and risks being either more or less than the levels presented in evidence. (Hazardous Substances and New Organisms (Methodology) Order 1998)."

Section 36: 'Minimum standards'

The HSNO Act requires that assessment of applications must always take place. In making a decision on new organisms, the Act requires the Authority to consider what could be called an environmental 'bottom line' in the form of minimum standards. These standards are reproduced from the HSNO Act below and it is extremely important that applicants understand and address these standards in the application:

"36. Minimum standards. The Authority shall decline the application, if the new organism is likely to:
(a) Cause any significant displacement of any native species within its natural habitat; or
(b) Cause any significant deterioration of natural habitats; or
(c) Cause any significant adverse effects on human health and safety; or
(d) Cause any significant adverse effect to New Zealand's inherent genetic diversity; or
(e) Cause disease, be parasitic, or become a vector for human, animal, or plant disease, unless the purpose of that importation or release is to import or release an organism to cause disease, be a parasite, or a vector for disease."

For biological control agents, the emphasis is mainly upon (a), (b), and (d).

Costs of application preparation

The time and cost of putting together an application to be submitted to the EPA should not be underestimated. Sufficient time should be allowed to optimise the chances of a favourable outcome. The applicant should consider the following before starting to complete the application form:

If these questions have been addressed then the applicant is in a good position to prepare the application. Sufficient time should be allowed to consider each section of the form very carefully.

Regulatory costs

Costs of processing an application which currently apply to biological control agents can be found on the EPA website [http://www.epa.govt.nz/about-us/fees/Pages/default.aspx].

Reference to the fee structure will show that fees for a non-notified containment application are very much less than for a notified application. However, note that a non-notified application is subject to the following consideration by the EPA:

"The Authority has discretion to notify the public of receipt of applications to import new organisms into containment. The default position is that receipt of such applications will not be publicly notified, unless there is likely to be significant public interest. Therefore, such applications may be processed either by the notified or non-notified paths, depending on the nature of the application. If the application is publicly notified, then it is subject to a public consultation process."

It is unlikely that a biological control agent would be processed under 'rapid assessment' provisions except under exceptional circumstances. The criteria which need to be met for this process to be adopted are:

"To be accepted under this rapid process, you need to provide sufficient scientific information that the 'release' of the new organism meets low risk criteria in the HSNO Act. For example:

In most cases the intention of releasing a biological control agent (e.g. for classical biological control) is that it would establish a self-sustaining population in the field. However, it is possible that a biological control agent intended for an inundative release could be made through this process.

Consultation with Māori

As part of the process of submitting an application to introduce a biological control agent, applicants are required to consult with Māori regarding any possible benefits or risks the proposed introduction may have on Māori culture and well being. Pre- application Māori consultation may be required. A useful checklist to assist with assessing an application for significance to Māori is Potential effects on outcomes of significance to Maori [http://www.epa.govt.nz/Publications/potential_effects_outcomes_significance_maori.pdf].

More advice on Māori engagement can be found at Te Hautu [http://www.epa.govt.nz/te-hautu/Pages/Te%20Hautū.aspx].

The need to consult with Māori on biological control applications

Introductions of biological control agents to New Zealand must be approved, through the EPA, under the HSNO Act. Section 6(d) of the Act [http://www.legislation.govt.nz/act/public/1996/0030/latest/DLM382993.html] requires that "the relationship of Māori and their culture and traditions with their ancestral lands, water, sites, wahi tapu [sacred places], valued flora and fauna, and other taonga [treasures]" be taken into account when applications are considered. Section 8 of the Act [http://www.legislation.govt.nz/act/public/1996/0030/latest/DLM382997.html] requires that the principles of the Treaty of Waitangi (Te Tiriti o Waitangi) are also taken into account. According to EPA policy, it is the responsibility of the applicants in the first instance to provide an assessment of risks, costs and benefits of the proposed introduction to Māori. If the proposed introduction is judged to be of significance to Maori, a process of consultation is required, the details and interpretation of which need to be included in the application. The purpose of the consultation process is to recognise and report all the relevant view points in good faith.

Applicants must demonstrate that they have made every effort to consult in a meaningful way with all of the appropriate groups. In considering the application, the EPA obtains advice on the Māori perspective from the EPA's Māori Policy and Operations Group, Kaupapa Kura Taiao. It is important to maintain contact with the Māori groups affected by the Decision after approval has been given, at the very least to provide them with annual updates on relevant activities and progress.

Significance of biological control to Māori

If the biological control agent under consideration has the potential to impact on native species, the natural environment, Māori cultural and spiritual values, or Māori health and well-being then a more detailed consultation process would be encouraged. A discussion with the EPA in the planning stages of the project is the best place to start.

The nature of consultation

"Consulting involves the statement of a proposal not yet finally decided upon, listening to what others have to say, considering their responses and then deciding what will be done." (Mr Justice McGechan, cited in 'Working with Māori under the HSNO Act; a Guide to Applicants'). However, opinions vary on the intent behind the word, and consultation can have negative connotations for Māori, as a result of bad experiences in some instances. Engagement is another term that is widely used, and refers to attracting and involving someone�s interest, rather than merely canvassing their opinions before making a decision. With regard to the process of consultation required by the EPA, engagement can be seen as the groundwork on which a meaningful formal consultation process can be conducted. The Ministry for the Environment has further useful information [http://www.mfe.govt.nz/publications/rma/guidelines-tangata-whenua-dec03/html/page4.html] and discussion of what constitutes effective consultation.

For the biocontrol researcher, facing limited funding and the huge technical and intellectual challenges of carrying out a biocontrol project, the need to engage with Māori can be daunting. Engaging and consulting with Māori for the purposes of an EPA application may require a biocontrol researcher to step outside their usual way of working to take into account the perspectives and opinions of a culture very different from that of the Western scientific culture in which they usually work. This can be personally challenging, and needs to be approached with respect and an open mind, as well as an awareness that the scientific viewpoint is only one of many possible interpretations of the world around us. The inclusion of spirituality in Māori protocol, in the form of prayers (karakia) or hymns (himene), may be challenging to some. Western culture maintains a strong separation between science and religion, to the extent that spiritual beliefs are very rarely expressed in science workplaces in New Zealand. Māori culture, however, can blend spiritual and supernatural considerations with knowledge of the natural environment. Where western science is traditionally reductionist, understanding the whole by examining the constituent parts, the Māori approach to science is holistic, understanding the whole through an understanding of relationships between the parts.

How to go about engagement and consultation

Details of the engagement and consultation process from the perspective of a biological control researcher are give in Table 2. Key points to remember are:

Table 2. The process of Māori engagement and consultation in relation to biological control.
Project milestoneMaori engagement and consultation suggestedPossible issues for Māori
Weed or pest problem identified, biocontrol identified as a possible solution.

Appoint a team member to take responsibility for Māori engagement issues throughout the project.

Read the EPA's documents on Māori engagement.

Take up opportunities to talk to Māori about the project wherever possible. Are there any opportunities for partnerships?

- Is the weed/pest valued by Māori?
- Does it provide food for native species?
- Is the weed or pest affecting native ecosystems, or other ecosystems valued by Maori?
Potential biocontrol agents identified and background information gathered.

Discuss with your organisation's Māori liaison person and the EPA .

- Is the proposed introduction of significance to Maori?
- What level of consultation might be needed?
- Who should introduce you to the right people? (this is very important!)

Ensure research team is aware of responsibilities to Māori. Consider training in Māori protocol, language and Treaty issues. Consider finding a consultant to facilitate engagement with Māori.

Early in the process discuss the project with the appropriate local Māori groups (generally those with mana whenua over the land around the research facility). Offer to talk to them about the project or biocontrol in general. Face-to-face meeting is important, so follow through with this if it is requested.

Record notes from meetings and phone conversations, and if possible get joint sign off of accuracy. Include these with the application when sending to the EPA.

If the agents were introduced could they:
- invade native habitats?
- affect native species?
- affect valued exotic species (e.g. Broom is a weed, but it provides food for keruru)?
- interbreed with native species (affect whakapapa)?
- reduce the need for pesticide sprays?
- help restore native ecosystems?

If a meeting is not requested, it could be due to lack of resources to host or attend a meeting, rather than lack of interest.

Determine non-target species for host range testing Talk to your Māori contacts regarding the contents of the list. EPA staff may be able to provide advice and suggest information sources for non-target species of interest to Māori. Prepare an article on the project in Māori-specific media, such as the EPA's Te Putara newsletter. Check if there are any relevant species that are:
- Taonga, such as those listed in the Ngai Tahu Settlement Act
- Rare or endangered
- Have medicinal value to Māori, or are a traditional source of food
- Valued exotic species
Prepare the EPA application to import into containment (if appropriate) Formally consult with hapu or iwi with mana whenua over the containment facility, according to EPA guidelines. Relationships developed earlier are important here. Ensure concerns and questions are followed up appropriately, and included in the application, as well as a description of the consultation process. - What are the risks of escape from containment?
- What plans are in place if this occurs?
- What could the impact be on native flora and fauna?

Ongoing communication is important, as is talking to the right people. Be open minded about opportunities to work together to mitigate cultural concern.

Submit EPA application to import into containment (if appropriate) Notify all groups consulted with that the application has been submitted, and what the process is for public submissions.
Approval given to import into containment (if appropriate) Maintain ongoing communication with your network of contacts by telling them about the outcome of the application process.
First shipment of organisms Ensure your contacts are informed when the first shipment is expected. Be open to holding a celebration or blessing ceremony if this is requested. Allow Maori to determine appropriate protocol for this.
Host range testing Keep lines of communication with your network of contacts open. Mutually agree on what amount of communication is appropriate during the research process.
Prepare EPA application to release

Formally consult with local Maori according to EPA guidelines. This should start at least 6 months before proposed submission. Start by discussing issues in person with your established local contacts. Ask them who it would be appropriate to contact among other hapu or iwi in the area. Through these contacts, contacts at a national level may be found. Discuss with the EPA the best way to approach consultation on a national level.

During the consultation process, always be open to meeting face to face to discuss the issues. It may be appropriate to present the results of your research at a hui. Discuss the consultation process with the EPA.

Ensure all concerns and questions are followed up appropriately, and included in the application. Ongoing communication is the key.

Who you consult with and how is important, and if done badly can damage relationships with Māori. Relationship building and honest and open engagement is important. Work through the appropriate networks, with the backing and guidance of local tangata whenua. Your organisation's Māori liaison person is invaluable for guiding the process of introducing you to the appropriate people, and guiding the engagement and consultation process.
Submit EPA application to release Notify all groups consulted with that the application has been submitted, and what the process is for public submissions.
Application hearing Where possible provide support, advice and information for Māori groups wishing to prepare submissions. The Maori Policy and Operations Group at the EPA can also provide support and advice to these groups.
Approval given to release Communicate the outcome of the hearing with your local Māori contacts. They may be interested to discuss what happens next. After this point there is no formal requirement to consult with Māori, but the process of engagement and relationship building is ongoing. This is an opportunity for partnerships to form, and new possibilities for research may arise to the benefit of both Māori and scientists.
First release of agent Communicate the intention to release the agent with your local contacts. Be open to their involvement in the first release - a blessing ceremony may be appropriate. Look into who has mana whenua over the land where the release will occur, and allow for their involvement in the process. This communication may go through the company that manages the land in some cases. The introduction of a new organism is a significant event, and Māori, as kaitiaki (guardians) of the land may wish to be involved in the process and mark the event.
Field trials Where appropriate, consult with Māori landowners of proposed field sites prior to release. Allow their decisions regarding the release to inform the choice of site (especially if management of the land is contracted out). If there is funding and opportunity, consider involving Māori landowners and communities in field trials. - What are the expectations for the agent at the trial stage?
- What are the risks?
- What happens if it goes wrong?
- How long until we know if it has worked or not?
Distribution by land managers Consider engaging with Māori communities to develop partnerships for the distribution of the agent. The role of Māori as kaitiaki (guardians) of their land may be threatened if they do not have control over or input into the release of a biocontrol agent on or near their land.
Ongoing monitoring of agents success Where possible maintain communication with local Māori contacts about the successes and failures of the project. This may be alongside the process of consultation for another biocontrol agent. Consider writing articles for national Māori-specific media such as the EPA's Te Putara newsletter. Knowledge of the results of past biocontrol releases is as valuable to Maori as it is to biocontrol scientists for judging the worth of future applications.

References

Askew R.R. and Shaw M.R. (1986). Parasitoid communities: their size, structure and development. Pp. 225-264 In: Insect parasitoids, J.K. Waage and D.J. Greathead (Ed.) Academic Press, London.

Aubert B. and Quilici S. (1983). Nouvel �quilibre biologique observe � la R�union sur les populations de psyllides apr�s l�introduction et l��stablissement d�hymenopteres chalcidiens. Fruits 38: 771-780.

Barbosa P. (1998). Conservation biological control. Academic Press, London.

Barratt B.I.P., Blossey B. and Hokkanen H.M.T. (2006). Post-release evaluation of non-target effects of biological control agents. Pp. 166-186 In: Environmental Impact of Arthropod Biological Control: Methods and Risk Assessment, U. Kuhlmann, F. Bigler and D. Babendreier (Ed.) CABI Bioscience, Delemont, Switzerland.

Barratt B.I.P., Evans A.A., Ferguson C.M., Barker G.M., McNeill M.R. and Phillips C.B. (1997). Laboratory nontarget host range of the introduced parasitoids Microctonus aethiopoides and Microctonus hyperodae (Hymenoptera: Braconidae) compared with field parasitism in New Zealand. Environmental Entomology 26: 694-702.

Barratt B.I.P., Evans A.A., Stoltz D.B., Vinson S.B. and Easingwood R. (1999). Virus-like particles in the ovaries of Microctonus aethiopoides Loan (Hymenoptera: Braconidae), a parasitoid of adult weevils (Coleoptera: Curculionidae). Journal of Invertebrate Pathology 73: 182-188.

Barratt B.I.P., Goldson S.L., Ferguson C.M., Phillips C.B. and Hannah D.J. (2000). Predicting the risk from biological control agent introductions: A New Zealand approach. Pp. 59-75 In: Nontarget effects of biological control introductions, P.A. Follett and J.J. Duan (Ed.) Kluwer Academic Publishers, Norwell, Massachusetts, USA.

Barratt B.I.P., Murney R., Easingwood R., Ward V.K. (2006). Virus-like particles in the ovaries of Microctonus aethiopoides Loan (Hymenoptera: Braconidae): comparison of biotypes from Morocco and Europe. Journal of Invertebrate Pathology 91: 13-18.

Bellows T.S. and Fisher T.W. (1999). Handbook of Biological Control: Principles and Applications of Biological Control. Academic Press, San Diego.

Caltagirone L.E. (1981). Landmark examples in classical biological control. Annual Review of Entomology 26: 213-232.

Caltagirone L.E. and Huffaker C.B. (1980). Benefits and risks of using predators and parasites for controlling pests. Ecological Bulletin 31: 103-109.

Cameron P., Hill R.L., Bain J., Thomas W.P. (1993). Analysis of importations for biological control of insect pests and weeds in New Zealand. Biocontrol Science and Technology 3: 387-404.

Carson R. (1963). Silent Spring. Hamish Hamilton, London.

Charudattan R. (2005). Ecological, practical, and political inputs into selection of weed targets: What makes a good biological control target? Biological Control 35: 183-196.

Civeyrel L. and Simberloff D. (1996). A tale of two snails: is the cure worse than the disease? Biodiversity and Conservation 5: 1231-1252.

DeBach P. (1974). Biological control by natural enemies. Cambridge University Press, London.

DeBach P. and Rosen D. (1991). Biological control by natural enemies. Cambridge University Press, Cambridge, UK.

Ehler L.E. (1990). Environmental impact of introduced biological control agents: implications for agricultural biotechnology. Pp. 85-96 In: Risk assessment in agricultural biotechnology, J.J. Marois and G. Breuning (Ed.) California Division of Agriculture and Natural Resources, Oakland.

ERMA New Zealand (1998). Annotated methodology for the consideration of applications for hazardous substances and new organisms under the HSNO Act 1996. ERMA New Zealand, Wellington, New Zealand. 28 pp.

Evans A.A., Barratt B.I.P. and Ferguson C.M. (1994). Susceptibility of legume and Hieracium spp. seedlings to feeding by native broad-nosed weevils (Coleoptera: Curculionidae). Pp. 206-209 In: Proceedings of the 47th New Zealand Plant Protection Conference, A.J. Popay (Ed.) Waitangi Hotel, Pahia, N.Z., New Zealand Plant Protection Society Inc.

Ferguson C.M., Cresswell A.S., Barratt B.I.P. and Evans A.A. (1998). Non-target parasitism of the weed biological control agent, Rhinocyllus conicus Froelich (Coleoptera: Curculionidae) by Microctonus aethiopoides Loan (Hymenoptera: Braconidae). Pp. 517-524 In: Pest Management - Future Challenges: Proceedings of the 6th Australasian Applied Entomological Research Conference, M. Zalucki, R. Drew and G. White (Ed.) The Cooperative Research Centre for Tropical Pest Management, Australia.

Fowler S.V. (2000). Trivial and political reasons for the failure of classical biocontrol of weeds: a personal view. Pp. 169-172 In: Proceedings of the International Symposium on Biological Control of Weeds, N.R. Spencer (Ed.) Bozeman, Montana.

Godfray H.C.J. (1994). Parasitoids: Behavioural and Evolutionary Ecology. Princeton University Press, Princeton. 473 pp.

Hawkins B.A. and Marino P.C. (1997). The colonization of native phytophagous insects in North America by exotic parasitoids. Oecologia 112: 566.

Holt R.D. and Hochberg M.E. (2001). Indirect interactions, community modules and biological control: a theoretical perspective. Pp. 13-37 In: Evaluating indirect ecological effects of biological control, E. Wajnberg, J. K. Scott and P. C. Quimby (Ed.) CABI Publishing, Wallingford, Oxon., UK

Hopper K.R. (1995). Potential impacts on threatened and endangered insect species in the United States from introductions of parasitic Hymenoptera for the control of insect pests. Pp. 64-74 In: Biological Control: Benefits and Risks, H.M.T. Hokkanen and J.M. Lynch (Ed.) Cambridge University Press, Cambridge, UK.

Howarth F.G. (1983). Classical biological control: panacea or Pandora's box. Proceedings of the Hawaiian Entomological Society 24: 239-244.

Howarth F.G. (1991). Environmental impacts of classical biological control. Annual Review of Entomology 36: 489-509.

Howarth F.G. and Ramsay G.W. (1991). The conservation of island insects and their habitats. Pp. 71-107 In: The Conservation of Insects and their Habitat, N.M. Collins and J.A. Thomas (Ed.) Academic Press, London.

Knudsen I.M.B., Hockenhull J., Jensen D.F., Gerhardson B., Hokeberg M., Tahvonen R., Teperi E., Sundheim L. and Henriksen B. (1997). Selection of biological control agents for controlling soil and seed-borne diseases in the field. European Journal of Plant Pathology 103: 775.

Lockwood J.A. (1993). Environmental issues involved in biological control of rangeland grasshoppers (Orthoptera: Acrididae) with exotic agents. Environmental Entomology 22: 504-518.

Louda S.M. (1999). Negative ecological effects of the musk thistle biological control agent, Rhinocyllus conicus. Pp. 213-243 In: Nontarget effects of biological control introductions, P.A. Follett and J.J. Duan (Ed.) Kluwer Academic Publishers, Norwell, Massachusetts, USA.

Louda S.M., Rand T.A., Arnett A.E., McClay A.S., Shea K. and McEacherne A.K. (2005). Evaluation of ecological risk to populations of a threatened plant from an invasive biocontrol insect. Ecological Applications 15: 234-249.

Nechols J.R., Kauffman W.C. and Schaefer P.W. (1992). Significance of host specificity in classical biological control. Pp. 41-52 In: Selection Criteria and Ecological Consequences of Importing Natural Enemies, W.C. Kaufmann and J.E. Nechols (Ed.) Entomological Society of America, Lanham, Maryland, USA.

Nowell D. and Maynard G.V. (2005). International guidelines for the export, shipment, import and release of biological control agents and other beneficial organisms (ISPM No. 3). Pp. 726-734 In: Second International Symposium on Biological Control of Arthropods, M. Hoddle (Ed.) Davos, Switzerland, USDA Forest Service.

Pearson D.E. and Callaway R.M. (2005). Indirect nontarget effects of host-specific biological control agents: Implications for biological control. Biological Control 35: 288-298.

Pimentel D. (1980). Environmental risks associated with biological control. Ecological Bulletin 31: 11-24.

Samways M.J. (1994). Insect Conservation Biology. Chapman & Hall, London. 358 pp.

Sands D.P.A. (1993). Effects of confinement on parasitoid-host interactions: interpretation and assessment for biological control of arthropod pests. Pp. 196-199 In: Pest Control in Sustainable Agriculture, S.A. Corey, D.J. Dall and W.M. Milne (Ed.) CSIRO, Canberra, Australia.

Schulten G.G.M. (1997). The FAO Code of Conduct for the import and release of exotic biological. Pp. 29-36 In: EPPO/CABI workshop on safety and efficacy of biological control in Europe, I.M. Smith (Ed.) Blackwell Science Ltd., Oxford.

Sheppard A.W. (1992). Predicting biological weed control. Trends in Ecology & Evolution 7: 290-291.

Simberloff D. and Stiling P. (1996). How risky is biological control? Ecology 77: 1965-1974.

Simmonds F.J. and Bennett F.D. (1977). Biological control of agricultural pests. Pp. 464-472 In: Proc. 15th International Congress of Entomology.

Simmonds F.J., Franz J.M. and Sailer R.I. (1976). History of biological control. Pp. 788 In: Practice of biological control, C.B. Huffaker and P.S. Messenger (Ed.) Academic Press, New York.

Stoltz D.B. and Xu D. (1990). Polymorphism in polydnavirus genomes. Canadian Journal of Microbiology 36: 538-543.

Strand M.R. and Obrycki J.J. (1996). Host specificity of insect parasitoids and predators. BioScience 46: 422-429.

van den Bosch, R., Messenger, P.S. and Gutierrez, A.P. (1982). An introduction to biological control. Intext Educational Publishers, Plenum Press, New York and London. Pp 247

van Driesche R.G. and Bellows T.S. (1996). Biological control. Chapman and Hall, New York. 539 pp.

van Emden H.F. (2003). Conservation biological control: from theory to practice. In: Proceedings of the 1st International Symposium on Biological Control of Arthropods, R. Van Driesche (Ed.) United States Department of Agriculture Forest Service, Washington, USA.

van Lenteren J.C. (1997). Benefits and risks of introducing exotic macro-biological control agents into Europe. Pp. 15-27 In: EPPO/CABI workshop on safety and efficacy of biological control in Europe, I.M. Smith (Ed.) Blackwell Science Ltd., Oxford.

van Lenteren J.C. (2000). Success in biological control of arthropods by augmentation of natural enemies. Pp. 77-103 In: Measures of Success in Biological Control, G. Gurr and S. D. Wratten (Ed.) Kluwer Academic Publishers, Dordrecht

Vinson S.B. (1990). How parasitoids deal with the immune system of their host: an overview. Archives of Insect Biochemistry and Physiology 13: 3-27.

Wapshere A.J. (1974). A strategy for evaluating the safety of organisms for biological weed control. Annals of Applied Biology 77: 201-211.

Webb B.A. and Summers M.D. (1990). Venom and viral expression products of the endoparasitic wasp Campoletis sonorensis share epitopes and related sequences. Proceedings of the National Academy of Sciences of the United States of America 87: 4961-4965.

Wells S.M., Pyle R.M. and Collins N.M. (1983). Large blue butterflies. Pp. 451-457 In: The IUCN invertebrate red data book, (Ed.) International Union for Conservation of Nature and Natural Resources, Gland, Switzerland.

Whitfield J.B. (1994). Mutualistic viruses and the evolution of host ranges in endoparasitoid Hymenoptera. Pp. 163-176 In: Parasitoid community ecology, B.A. Hawkins and W. Sheehan (Ed.) Oxford University Press, Oxford.

Willis A.J. and Memmott J. (2005). The potential for indirect effects between a weed, one of its biocontrol agents and native herbivores: A food web approach. Biological Control 35: 299-306.