Food Sec. (2010) 2:49–70 DOI 10.1007/s12571-010-0054-7

ORIGINAL PAPER

Evolution of the international regulation of plant pests and challenges for future plant health Alan MacLeod & Marco Pautasso & Mike J. Jeger & Roy Haines-Young

Received: 9 November 2009 / Accepted: 12 January 2010 / Published online: 23 February 2010 # British Crown Copyright 2010

Abstract Plant pathogens and invertebrates harmful to plants, collectively referred to as plant pests, continue to threaten food security. International cooperation and regulatory systems to inhibit the spread of plant pests began formally in 1878. Initially seven countries worked together and agreed phytosanitary measures against grape phylloxera, Phylloxera vastatrix (=Daktulosphaira vitifoliae). There are now 172 countries that are contracting parties to the International Plant Protection Convention, a treaty that aims to prevent the introduction and spread of pests of plants and plant products, and to promote appropriate measures for their control. Apparently contradictory interests between international trade, which has facilitated the spread of plant pests, and the protection of plants are mutually recognised in global trade and phytosanitary agreements. The principle that risk management measures should provide an appropriate level of protection without undue interference in trade was established within the plant protection agreements at the beginning of the 20th Century and is still fundamental to risk management policy today. Globally ten Regional Plant Protection Organizations

facilitate more local cooperation and recommend the regulation of over 1,000 named quarantine plant pests. Member States of the European Union work together and regulate imported plant material on the grounds of plant health with each Member State taking into account the plant health concerns of every other Member State. However, decision making can be slow and border inspections poorly targeted. Close relationships between regulatory scientists and policy makers, focussed on agricultural and horticultural production, are changing to take a broader stakeholder community into consideration as decisions regarding the environment seek to draw upon a wider knowledge base. Challenges that impede the success of limiting international pest movement include increased international trade and climate change. International guidelines designed to prevent pest spread present challenges of their own if they remain difficult to implement. Keywords Pest risk analysis . Phytosanitation . Plant biosecurity . Quarantine . Regulatory science

Introduction A. MacLeod (*) The Food and Environment Research Agency, Sand Hutton, York YO41 1LZ, UK e-mail: [email protected] M. Pautasso : M. J. Jeger Division of Biology, Imperial College London, Silwood Park, Ascot SL5 7PY, UK R. Haines-Young Centre for Environmental Management, School of Geography, University of Nottingham, Nottingham NG7 2RD, UK

Throughout history societies have incurred crop losses caused by plant diseases and invertebrate pests leading to food shortages and hardship. Today, impacts of plant pests and pathogens still range from slight damage or mild symptoms to major catastrophes in which large areas of food crops and semi-natural vegetation are destroyed (Oerke et al. 1994; Scholthof 2003; Holdenrieder et al. 2004; Strange and Scott 2005) and there is a need to integrate knowledge of plant pests and pathogens into the food security and climate change debate (Butterworth et al. 2009; Gregory et al. 2009; Miraglia et al. 2009). Given that

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the world’s population is expected to reach 9 billion by 2045 (US Census Bureau 2009) the importance of reducing losses from pests and diseases is as important as ever. Diseases that directly affect crop yield and disrupt the food chain can impact on land use and social infrastructure (Aalen et al. 1997). For example, coffee leaf rust, caused by the pathogen Hemileia vastatrix, so devastated Sri Lankan coffee production that as an industry it became uneconomic and was eventually abandoned (Kushalappa and Eskes 1989). This and other classic examples of plant disease impacts are described in the very accessible text by Large (1940). Campbell et al. (1999) provide examples with a focus on the USA. Oerke et al. (1994) examined pest induced losses in major food crops globally and estimated that without protection diseases could cause 17% losses in wheat, whilst animal pests could cause 11% losses. More recently pests and plant diseases are seen as having wider impacts on ecosystem services, for example directly through destruction of service providers, or indirectly as a consequence of their management (e.g. Cheatham et al. 2009). Faced with such potential impacts, efforts to protect plants have historically focussed on securing food supply, preventing catastrophic events such as famine, or preventing farmers from suffering significant financial losses (Fry 1982; Hadidi et al. 1998; Meester et al. 1999). As scientific understanding and knowledge about the causes and impacts of plant pests and diseases have developed, so too have national and international efforts to control them. This review describes in some detail how the existing arrangements for the international regulation and management of non-native plant pests arose and have evolved over

the past 120 years. We demonstrate the evolution by noting developments of key international treaties and illustrate changes within selected national and regional bodies responsible for plant health. Changes in social values, attitudes and expectations have also occurred such that regulators can take a broader view of pests and consider their impact in the natural environment. The challenges posed by the drivers responsible for continued pest spread are noted together with institutional challenges. To assist readers new to this area of regulatory science, a guide to the abbreviations used within the text is provided (Table 1). In the literature, newly arrived species are variously referred to as “alien”, “exotic”, “introduced”, “invasive”, “transboundary”, “non-indigenous” or “non-native” (Williamson 1996; Mack et al. 2002). These terms are occasionally used interchangeably. “Harmful organism” and “pest” can also appear synonymous. Efforts to define and standardise such terminology have been made (e.g. Colautti and MacIsaac 2004; Ereshefsky 2009; FAO 2009). Pest, for example is defined in FAO (2009) as “any species, strain or biotype of plant, animal or pathogenic agent injurious to plants or plant products”. Such a definition clearly covers invertebrates and disease causing pathogens and is used in the text from this point.

What is plant health? Plant health is first of all the health, i.e. well-being, of individual plants and communities, together with their associated organisms, both in (semi)natural and cultivat-

Table 1 Abbreviations used in the text Abbreviation

Full name

Website

CBD CPM EC EFSA EPPO EU FAO FVO IPPC ISPM NPPO

Convention on Biological Diversity Commission on Phytosanitary Measures European Commission European Food Safety Authority European and Mediterranean Plant Protection Organization European Union Food & Agricultural Organization of the United Nations Food and Veterinary Office of the EC International Plant Protection Convention International Standards for Phytosanitary Measures National Plant Protection Organization

RPPO SASA SCPH SPS WTO

Regional Plant Protection Organization Science and Advice for Scottish Agriculture EC Standing Committee on Plant Health Agreement on the Application of Sanitary and Phytosanitary measures World Trade Organization

http://www.cbd.int/ https://www.ippc.int/index.php?id=13330 http://ec.europa.eu/index_en.htm http://www.efsa.europa.eu/ http://www.eppo.org/ http://europa.eu/ http://www.fao.org/ http://ec.europa.eu/food/fvo/index_en.cfm https://www.ippc.int/ https://www.ippc.int/index.php?id=13399&L=0 https://www.ippc.int/index.php?id=1110520&no_ cache=1&type=contactpoints&L=0 https://www.ippc.int/index.php?id=13310&L=0 http://www.sasa.gov.uk/ http://ec.europa.eu/food/fs/rc/scph/index_en.htm http://www.wto.org/english/tratop_e/sps_e/sps_e.htm http://www.wto.org/

Evolution of the international regulation of plant pests

ed ecosystems (Cook 2000; Ostry and Laflamme 2009; Tollefsen et al. 2009). However, from a biosecurity perspective, and for the purposes of this text, plant health is a term which refers to the legislative and administrative procedures used by governments to prevent plant pests from entering and spreading within their territories (Ebbels and King 1979). Plant health includes activities sometimes referred to as “plant quarantine”. However, plant health goes further to include health standards in schemes for production and marketing of healthy planting material, referred to as “certification schemes” (Ebbels 1993). Many horticultural crops are vegetatively propagated, potentially allowing pathogens to be transmitted to progeny. Effectively implementing schemes that describe how best to multiply and test plants to provide healthy planting material can be an important part of pest control and plant health risk management (Roy 2009). Equally important can be the management and disposal of infested plant waste (Noble et al. 2009). Plant health can be regarded as a distinct component of crop protection. Typically crop protection is managed locally by growers who seek to minimise pest impacts on individual businesses. In contrast plant health is managed nationally by governments which seek to minimise the impact of exotic plant pests within their territories (Trevelyan 1993). Traditionally plant health has focussed on pests which are potentially harmful to agricultural, horticultural and forestry industries i.e. crops (Ebbels and King 1979). However, during the 1990s and early 21st Century, government departments and ministries have shifted from a focus on production towards natural resource management and environmental protection. Consequently plant health has increasingly reached out to act against plant pests that potentially threaten the wider environment (IPPC Secretariat 2005b; Hallman 2007; Holmes et al. 2008; Cheatham et al. 2009; Kelly and Bliss 2009). New Zealand exemplifies such an approach following the implementation of its Biosecurity Act of 1993, designed among other things to protect all of New Zealand’s plant resources. However, agricultural production and food security issues are gaining media attention and moving back up the political agenda once again (Defra 2008a; Ambler-Edwards et al. 2009; Frow et al. 2009; House of Commons Environment, Food and Rural Affairs Committee 2009; Pinstrup-Andersen 2009).

History of plant health regulation and international agreements up to 1951 17th Century Perhaps the first phytosanitary legislation was in 17th Century Europe when the legislative authorities of Rouen, France, passed a law in 1660 requiring the destruction of

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barberry (Berberis vulgaris) bushes in wheat growing areas to protect wheat from a disease, later identified as black stem rust caused by Puccinia graminis (Ebbels 2003; Dubin and Brennan 2009). In countries, such as the UK, where black stem rust was not so important, destruction of barberry was left as a voluntary action, although it was sometimes encouraged. 18th & 19th Century The pioneering biologist Carl Linnaeus hinted at the need for quarantine in the 18th Century (Usinger 1964) even at a time when only comparatively small quantities of plants were carried all over the world without restrictions. Inevitably such movements carried plant pests too. However, without an understanding of plant pathology, the principles of plant quarantine were not identified as a means of mitigating the risks. Working on wheat smut (wheat bunt), Isaac-Benedict Prevost, a founding father of plant pathology, was the first to demonstrate experimentally that plant diseases were caused by micro-organisms (Prévost 1807). This was 25 years ahead of the first experimental proof that animal diseases were caused by pathogens. Prior to Prevost’s experiments it was generally believed that any fungi associated with plant disease were derived from diseased plant tissue through spontaneous generation (Ainsworth 1981). The Irish potato famine of the 1840s is generally regarded as the point in time when plant pathology became recognised as a science in its own right. The famine occurred approximately 200 years after the introduction of potato from South America into Europe. There are many explanations as to the cause of the famine, but a primary factor was the over reliance on a single potato variety, cv. Lumper, that was particularly susceptible to the pathogen responsible for potato blight, Phytophthora infestans. However, it was not until several years later that de Bary (1861, 1865) firmly showed that P. infestans was the causal agent. Disease impacts were made worse by a lack of support by Anglo-Irish landowners (Salaman 1985). The disease also occurred at the same time in the Netherlands and elsewhere in Europe but the impact was not as serious (Koeman and Zadoks 1999). The last major famine due to P. infestans was in Germany in 1916 when 700,000 civilians died. Copper that could have been used in fungicide against the pathogen was instead used to manufacture bullets for use in war (Schumann 1991). Other introduced plant diseases of concern in Europe during the later half of the 19th Century included Oidium (a mildew) of grapevine (1847) and Guignardia bidwelli (black rot) of grape (1888). During the same period in North America Cronartium pine rusts (1883), chestnut blight, Cryphonectria (Endothia) parasitica (1904) and bacterial canker of

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citrus, Xanthomonas citri (1912) were causing major impacts (Mathys and Baker 1980). The first international agreement to prevent the spread of a plant pest was put in place against an insect pest of grape vines. Daktulosphaira vitifoliae, then known as Phylloxera vastatrix, was accidentally introduced into Europe when a French wine merchant imported infested US vines for hybridization to his Rhône vineyards in 1862. Infested vines were also shipped to Australia (Maynard et al. 2004) and South Africa (Vanzyl 1984) at the same time, spreading the pest further. Phylloxera was also spread from California to New Zealand and Peru (Downie 2002). North American grape varieties were tolerant to the hemipteran pest, which formed galls on their immature roots and leaves. However, in Europe, Australia and South Africa the pest formed galls on mature storage roots and allowed secondary pathogens to infest the plants, ultimately killing the vines. Seven European countries suffering from the pest met in Berne, Switzerland in 1878, to discuss how to tackle the problem. They developed the International Convention on Measures to be taken against Phylloxera vastatrix, which was signed in September 1878 (Ebbels 2003). The Convention described several measures such as: providing written assurance of the Phylloxera free status of host material traded internationally, powers to inspect material and to take action on non-compliant material, and the requirement to establish an official government body to administer the implementation of such a system. An English translation of the Convention is provided in Ebbels (2003). Unfortunately the Convention used terms that were not clearly defined and, 3 years later, the countries again met in Berne and a revised Convention was signed in November 1881 containing definitions.1 By 1884 over 1 million hectares of French vineyards had been destroyed and over 0.6 million hectares were severely infested. The French government offered a huge reward to anyone who could cure the problem (Campbell 2004). In Sydney, Australia, port inspections of cargo, including plants, began in 1889 (Australian Academy of Science 2003; Maynard et al. 2004), the same year that a third Convention was signed, once more in Berne.

similar calls at various international meetings it was not until 1903 that a special international committee for plant diseases was formed at the Seventh International Agricultural Congress (Rogers 1914). However, the committee was composed of academic scientists and no governments were represented. The first step taken jointly by governments was in June 1905 with the formation of the International Institute of Agriculture (IIA) in Rome. The IIA made studies of international agriculture with particular reference to agricultural techniques, statistics, economics and legislation. It published monographs, monthly bulletins and international yearbooks. The next milestone was the 1914 International Phytopathological Conference held in Rome. This event was very much driven by the French government, who had organised it, and who presided over it; French technical delegates also took very prominent roles. Thirty countries were represented. Some countries unable to attend had accepted in advance the need for an international convention. The British delegation aimed to include five specific points in any international convention that resulted from the meeting.

Late 19th and early 20th Century

&

At the International Congress of Agriculture and Forestry in 1890, eminent plant pathologists called for an International Phytopathological Committee. This was not the first call for international action on plant diseases, which appears to have come from Eriksson in 1880 (Rogers 1914). Despite

Within 2 years contracting parties were required to have established one or more institutes for research so that government could access high quality scientific and technical advice. Grains, seeds, potatoes, onions and general farm produce were excluded from the Convention because it was felt that including such commodities that were already heavily traded would overwhelm the inspection systems already in place and which already provided some protection.

1 The 1881 Convention is often (mistakenly) cited as the first international plant protection agreement, when in fact it is clearly a revision of the original 1878 Convention.

1. that plants traded internationally from a nursery should be officially inspected and found free from important diseases, 2. that the plants should have an official certificate of health, 3. that the health certificate should specify the diseases for which an examination had taken place, 4. that it should not be necessary for every consignment to be inspected, 5. that consignments with health certificates should not be delayed at border frontiers for inspection (Rogers 1914). The first four aims were apparently easily agreed to but the fifth was not achieved since countries would not agree to entirely give up the right to examine consignments on arrival. If countries signing up to the Convention had not already established a number of plant health procedures they were, amongst other things, required to immediately: & & &

establish an official inspection service for businesses that market plants; issue health certificates to plants that had been inspected and found free from specified pests; control plant movements, their packing and transport; and, organise a service to suppress dangerous diseases.

Evolution of the international regulation of plant pests

It was agreed that each country should compose its own list of pests against which it wished to be protected. In order to justify being placed on such a list, it was agreed that host plants must be present in the country; that the pest could not be widespread; the pest must be able to survive on a trade pathway; and finally that the pest should be injurious to the plant, where injurious meant destructive to the commercial value of the crop. Such criteria remain at the centre of plant health thinking today. Of note, the convention was probably the first to link scientific research with government administration, adding weight and prestige to scientists’ efforts. Early plant health policy was clearly aimed at specific pests considered to be of particular concern due to the potential damage and the apparent threat of entry. The later 1929 International Convention for the Protection of Plants expanded on concerns over Phylloxera to include other problematic species. At this time, the number of countries participating in such international plant protection meetings had grown from the original seven in 1878 to 46 in 1929. Unfortunately, despite the increased interest in this area, only 12 countries ever ratified the Convention and events surrounding World War II meant that the 1929 Convention was not an effective instrument (Mulders 1977). During WWII, 44 governments meeting in the United States committed themselves to founding a permanent organization for food and agriculture. Consequently, after WWII ended, the IIA was dissolved and its functions and assets transferred to the Food and Agricultural Organization (FAO) that was established in 1945 as a specialized agency of the United Nations (UN) (FAO 2008). During the first 5 years of the FAO’s existence, member countries submitted proposals for an international plant protection agreement. A draft agreement, synthesized from the representations, was considered at a meeting of FAO in The Hague in 1950 (Mulders 1977). The draft proposal was further developed by plant protection specialists from the USA and Canada. Following comments received during wider consultation the final draft of the International Plant Protection Convention (IPPC) was eventually agreed in September 1951 and adopted during the sixth session of the FAO Conference in Rome in November 1951 (Chock 1979; Ebbels 2003).

The International Plant Protection Convention since 1951 and related international agreements IPPC, 1951 The IPPC is an international treaty on plant health that aims to secure action to prevent the introduction and spread of pests of plants and plant products, and to promote appropriate measures for their control. As of December 2009 there were 172 contracting parties to the Convention.

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Just as the original Convention against Phylloxera was designed to prevent international movement of a pest and promote measures for pest control, the current Convention has similar aims. The IPPC provides a framework for international cooperation between National Plant Protection Organizations (NPPOs), the official (government) bodies responsible for IPPC obligations. Contracting parties follow IPPC principles, such as: & & & &

&

necessity (phytosanitary measures are only applied when necessary); technical justification (measures must be technically justified); transparency (measures must be published and the rationale for measures provided to other contracting parties if requested); non-discrimination (measures must be applied equally to countries of equivalent plant health status and to the same pest whether associated with imported goods or within the territory of the contracting party); and, minimal impact (measures applied must be commensurate to the assessed pest risk and be the least trade restrictive) (FAO 2002).

The IPPC is governed by the Commission on Phytosanitary Measures (CPM) and each NPPO may send representatives to sit on the CPM and to help direct its work. IPPC work falls into three general categories: 1. Setting standards: International Standards for Phytosanitary Measures (ISPMs) aim to reduce the spread of pests and facilitate trade through harmonizing phytosanitary measures applied in international trade. Examples of ISPMs include, “Phytosanitary principles for the protection of plants and the application of phytosanitary measures in international trade”, ISPM No. 1 (FAO 2006), and “Pest risk analysis for quarantine pests including analysis of environmental risks and living modified organisms” ISPM No. 11 (FAO 2004). Adopted standards are available via the IPPC website (Table 1). Although the IPPC itself is a legally binding agreement, ISPMs are not; they are guidelines that can be interpreted in different ways. As a result disputes between nations can arise. If disputes are not settled bilaterally they can escalate and ultimately may have to be resolved through the World Trade Organization (WTO). For example, the USA disputed measures Japan had in place restricting imports of apples based on the risk of transmission of Erwinia amylovora, the pathogen causing fire blight. The WTO ultimately found that the measures in place were “without sufficient scientific evidence” and disproportionate to the risk. Consequently Japan had to revise its import requirements (Goh 2006).

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In recent years three or four new standards have been produced each year. The majority of ISPMs are concept standards which can be seen as providing foundations for more specific and commodity focused standards. For example, ISPM 15 describes phytosanitary measures to reduce the risk of introduction and/or spread of quarantine pests associated with wood packaging material. Diagnostic standards are currently being planned. Development of international standards for commodities such as pome fruit, stone fruit or cut flowers would remove the need for individual countries to establish their own standards. The equivalent organization in animal health, the Office International des Epizooties (OIE) takes a commodity based approach in developing its standards and has standards for international trade in beef, pigmeat, poultry meat and milk (OIE 2009). However, it must be recognised that the OIE has very many fewer pests and diseases to concern itself with, than the very large number of plant pests of concern to plant health authorities. 2. Sharing information: Through the IPPC web-site, countries can share their phytosanitary regulations and information on the distribution of quarantine pests in their territory. However, very often reports by nongovernment scientists will highlight the expansion of the distribution of a pest before it is notified via the IPPC website. The occurrence of a quarantine pest in a country can lead to trading partners imposing import bans of host commodities (MacLeod et al. 2004), perhaps explaining the reluctance of countries to officially confirm the presence of some pests. 3. Technical assistance: Technical assistance can be provided to help countries implement the IPPC. Assistance can take the form of providing training courses and workshops, e.g. on practical implementation of ISPM 15 (IPPC Secretariat 2005a), invasive alien species (IPPC Secretariat 2005b) and pest risk analysis (IPPC Secretariat 2006). Technical assistance can also be provided through the development of documents to further explain standards, such as Supplement 1 to ISPM No. 11 (FAO 2003). As with previous plant protection Conventions, over time, revisions have been made, e.g. in 1979 and 1997 (FAO 1997, 2002). The day-to-day management, communication, co-ordination and information sharing is handled by the very small IPPC Secretariat in Rome. Unlike the independent OIE, the IPPC sits within the FAO. The IPPC Secretariat bears a heavy work load and lacks sufficient resources, both in staff numbers and technical ability, hence the reliance on technical skills provided by members of working groups and panels from contracting parties. With a larger technical staff, dedicated to the development of standards, the average time for standard development could

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be reduced from the current minimum of 5 years (IPPC 2007). However, there is little to gain from producing ever more standards if contracting parties lack the capacity to implement them. Future ISPMs should come with a guide on best practice for their implementation and, in order to enable them to be applied in a cost-effective manner, more resources should be made available to support contracting parties. Convention on biological diversity (CBD), 1992 The CBD is designed to safeguard biodiversity, ensure its sustainable use and share the benefits obtained from genetic diversity. The CBD and IPPC use different terminology although the IPPC definition for a quarantine pest can overlap with what the CBD refers to as an invasive alien species, defined as a species whose introduction and/or spread threaten biological diversity. The CBD refers to the risks of moving plants and other species between countries hence the IPPC and the CBD share and recognize some common ground and seek to find ways to cooperate, e.g. IPPC Secretariat (2005b). Invasive alien plants or weeds represent a significant area of mutual concern between the CBD and the IPPC (Schrader and Unger 2003). A second component to the CBD is the Cartagena Protocol on Biosafety (CBD 2000), an agreement on the use of genetically modified organisms, some of which may be plants or plant pests, and which may then overlap with IPPC concerns. SPS agreement, 1995 The IPPC makes provision for international trade within a plant protection agreement. Complementary provisions for plant protection within a trade agreement are made by the WTO in the Agreement on the Application of Sanitary and Phytosanitary Measures (WTO 1995), the so-called SPS Agreement (which also includes considerations of human and animal health). These agreements seek to achieve the same ends from different directions (Lopian 2005). The WTO is the 1995 reincarnation of the General Agreement on Tariffs and Trade (GATT) talks, which represent long-term global trade negotiations that seek to break down barriers and help to stimulate world trade (Durand and Chiaradia-Bonsquet 1999; Anon. 2004). Many factors contribute to the threat from exotic plant pests: increasing world trade, population mobility and tourism, an increase in information, communication, technology and wealth in developed countries which creates a demand for exotic plant material; habitat fragmentation, which may increase vulnerability; and, generally, the tendency towards the globalization of the world economy (DeGraaf 1994; Shogren 2000). Waage and Mumford (2008) abbreviate

Evolution of the international regulation of plant pests

these as the “four Ts” (trade, travel, transport and tourism). Indeed globalization through trade is argued to be the fundamental human cause of invasive non-native pest introductions (McNeely 1999; Perrings et al. 2000, 2002; Pimentel 2002; Taylor and Irwin 2004; Koo and Mattson 2004). Undoubtedly international trade has grown significantly since the middle of the Twentieth Century (WTO 2007). At the same time the international movement of plants has also increased. The development of trade routes has opened up new pathways for plant pests and potentially invasive species, and increased the frequency of introductions (Bandyopadhyay and Frederiksen 1999; Ruiz and Carlton 2003; Anderson et al. 2004; Caton et al. 2006; McCullough et al. 2006; Gullino and Garibaldi 2007). However, Jones and Baker (2007) did not find any significant variation in the frequency or rate of introductions of plant pathogens into the UK between 1970 and 2004, despite an increase in imports over this period. The authors speculated that this may have been due to improvements in the health status of imports, or the effectiveness of inspection procedures at entry. Waage and Mumford (2008) and Waage et al. (2008) point out that there has been little research into the patterns of pest introductions and although it may be straightforward, for example, to correlate increased trade with more pest introductions, there is little evidence for causation. One of the roles of the WTO is to facilitate world trade and the concomitant exchange of goods/commodities and services. However, the WTO recognises that there can be risks associated with trade, especially when biological entities are shipped internationally, so that species are moved to regions where they are non-native. The WTO addresses the concerns of the movement of non-native species within the SPS Agreement (WTO 1995). Article 5 of the SPS agreement states that risk assessment protocols developed by relevant international bodies should be used, as appropriate to the circumstances, to determine the risks associated with trade and to develop protective measures to mitigate the risks. Protective measures should, amongst other things, be scientifically based and be as unrestrictive of trade as possible (Anderson et al. 2001; McRae and Wilson 2002). To account for the extensive and persistent uncertainty around pests that can be spread internationally the WTO promotes learning, encourages monitoring of outcomes, encourages transparency, facilitates broad participation in policy-making processes, and highlights the limitations of the knowledge used to inform policy (Cooney and Lang 2007). Following the establishment of the WTO and the SPS Agreement, the FAO recognised that plant protection legislation would be significantly impacted, particularly with respect to trading practices, with consequences for food security (Durand and ChiaradiaBonsquet 1999) given more rigid conditions might be applied before commodities could be shipped. The WTO recognises

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the IPPC as the relevant body to develop risk assessment protocols for plant health. While the SPS Agreement implies the need for technical justification and non-discrimination, the IPPC sets out these concepts as detailed principles (Hedley 1992; Smith 1999). In theory the SPS Agreement and the IPPC provide a framework for a multilateral trading system in plants and plant commodities (van der Graaff 1999) but in practice trading partners may still have to arrange bilaterally how IPPC standards are to be applied in practice (Smith 1999). Figure 1 illustrates where these international bodies and agreements overlap and interact. Whilst Fig. 1 shows the inter-relatedness of three major international agreements protecting plant health, there are nearly 50 international legal instruments or guidelines that deal with the related but wider issue of invasive alien species (Shine 2007).

Economic rationale for government intervention At the local scale, combating plant pests is an economic necessity for farmers and decisions are generally made by individual growers. Pest prevention is based on good agronomic practice, rotation, use of pest free seed (which could be assured through certification systems organised by the NPPO), breeding for resistance to pests, good nutrient and water balance, and ensuring that plants do not become stressed and vulnerable. However, for non-native pests that threaten crops or plants in the wider environment or even plants in other countries, government intervention can be justified economically. Perrings et al. (2002) argue that the primary driver of the introduction of non-native species, resulting in some becoming invasive pests, is economics. Therefore, any analysis of the process from potential introduction to invasiveness must consider the economic infrastructure in Plant protection Protecting wild flora LMOs identified as pests

No more trade restrictive than necessary

LMOs Biological diversity Trade Trade while protecting biodiversity From an original diagram by Lesley Cree, Canadian Food Inspection Agency

Fig. 1 Links between international agreements protecting plant health. Key: IPPC = International Plant Protection Convention, SPS = WTO Agreement on the Application of Sanitary and Phytosanitary measures, CP = Cartagena Protocol on Biosafety, CBD = Convention on Biological Diversity, LMOs = Living Modified Organisms

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order to provide long-term solutions. With knowledge of the growing environment and management practices employed, export growers may well be aware of the health status of their plant products. However, this is not the case for importers since it can be difficult to detect plant pests and assess plant health condition. Thus it may be only after a period of time that a judgement can be made as to the quality of the material. In economic parlance, such a situation is referred to as information asymmetry, and is typical for “post-experience goods” (Boardman et al. 1996) which can cause market failure. If importers cannot easily identify pests in plants and plant products, and assuming that higher levels of plant health (e.g. pest freedom) are more costly to achieve due to quarantine treatments, then there will be an incentive for exporters to supply riskier products (Akerlof 1970). Negative externalities, e.g. damaging impacts to crops and the environment by pests introduced via plant imports for which the importer bears no cost would also be present. Hence, there is a role for government to intervene to ensure some form of quality assurance is provided. Infrastructures and services to protect against non-native pests are a public good that can only efficiently be provided by government (Temple et al. 2000). In a review of Australian quarantine, Nairn et al. (1996) recognised that commercial businesses would not choose to provide plant health services. More significantly it is governments that sign the relevant international agreements and only governments can take certain regulatory actions under such international agreements. There are many ways in which government can intervene. In the phytosanitary arena, these include establishing a plant protection service to impose phytosanitary regulations, to organise quarantine services, to conduct research, to collect and provide information and to administer voluntary schemes (Temple et al. 2000).

A national example of the evolution of plant health regulation Great Britain: late 19th and early 20th Century To illustrate the issues at a national level we review plant health regulation in Great Britain. Having established the rationale for government intervention, the history of plant health regulation in Britain began in August 1877 with the Destructive Insects Act. This had the objective of preventing the introduction and establishment of the major potato pest Leptinotarsa decemlineata (Colorado potato beetle). At the time L. decemlineata was known to have spread rapidly in the US. It had been found in Continental Europe in 1876 and, when a single beetle was found at Liverpool docks in 1877, it was clear that there was a pathway for

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entry of the pest into the UK (Bartlett 1979). Thirty years later the legislation was extended to cover other insects and fungi that were plant pests, although the Destructive Insects and Pests Act of 1907 was mainly intended to prevent entry of Sphaerotheca mors-uvae (American gooseberry mildew) on imported plants (Ebbels and King 1979). Plant pathogenic bacteria and viruses were first included in British plant health legislation 20 years later in the Destructive Insects and Pests Act of 1927. As part of the measures to control potato wart disease, a seed potato certification scheme was started in 1918 (Ebbels 2003). Great Britain: later 20th Century All the Acts were subsequently consolidated in the Great Britain Plant Health Act 1967 (Trevelyan 1993). The Act of 1967 recognised three competent authorities responsible for plant health. In England and Wales the Minister of Agriculture Fisheries and Food was responsible for agricultural and horticultural material; in Scotland it was the Secretary of State, whilst the Forestry Commissioners were responsible for forest trees and timber in Scotland, England and Wales. Ebbels (2003) described the rather fragmented nature of the UK National Plant Protection Organization (NPPO), noting its federal composition and how administrative and technical services are provided for phytosanitary services in England, Scotland, Northern Ireland, Wales, the Channel Islands and Isle of Man. In England and Wales plant health service scientists within the Food and Environment Research Agency (Fera), an executive agency of the Department for Environment Food and Rural Affairs (Defra) conduct research to improve methods of pest detection, identification and diagnosis (e.g. Hughes et al. 1997; Lane et al. 2007; Boonham et al. 2008); evaluate the threat from exotic pests through risk assessment (Baker et al. 2005), identify research needs to reduce uncertainty in such assessments (Sansford 1999; Sansford et al. 2008) and evaluate pest risk management measures (Cannon et al. 1999, 2007). Resulting information is shared with stakeholders via mail shots and increasingly via official websites.2 Similar work is performed in Scotland by SASA (Science and Advice for Scottish Agriculture). Despite the apparent complex organizational arrangements for plant health in the UK, Brasier (2008) concluded that the UK system works reasonably efficiently and operates to a high standard, although its focus on only regulating organisms that are already recognized pests was now questionable and that more attention should be paid to exotic species, not yet known to be harmful. However, regulators need to consider the “weight of evidence” before allocating scarce public 2 Fera Plant Health website: http://www.fera.defra.gov.uk/plants/plant Health/.

Evolution of the international regulation of plant pests

resources to protect plant health. Incursions of known pest species will demand regulators’ attention as a priority over the arrival of organisms with no history of being harmful. Nevertheless, there may be a role for species traits analysis to be used to identify potential pests (Leung et al. 2002; Kenis et al. 2007). At the time when international efforts to control the spread of plant pests first began to be discussed, Britain was the world’s leading trading nation, shipping commodities around the globe (Chapman 1992). At the same time, Britain was at the forefront of the early development of international agreements on plant protection. Given that trade is largely responsible for the spread of plant pests internationally, these two apparently contradictory interests have been balanced by the UK consistently taking a pragmatic approach, advocating that measures should provide a sufficient level of plant health protection without undue interference with trade. This principle, which the UK wished to ensure became established within the plant protection agreements at the beginning of the 20th Century, is still fundamental to the IPPC 100 years later. More formally such an approach is considered as managed risk. A key component of providing well-informed risk management measures is to a have a well-informed assessment of risk, which consists of an assessment of likelihood and consequence (MacLeod 2007). As shown above, early plant health policy was aimed at specific pests but legislation was later expanded to include other species of concern. Most countries developed their phytosanitary legislation in a similar way, first focusing on individual pests before creating more general legislation (Temple et al. 2000). In the USA it was individual States that led the development of plant health regulation with the Michigan Yellows Law of 1875, targeting Peach yellows phytoplasma, being an early example. Not until the Plant Quarantine Act of 1912 was there federal legislation covering many pests (Ainsworth 1981). European integration When the United Kingdom joined the European Community in 1973, plant health regulations were still fundamentally a national responsibility and there was little in the form of an integrated European strategy towards plant health within the single market. Therefore the 1967 Act continued to be the principal legal instrument providing plant health protection in Britain. Forty-one statutory instruments made under various acts were consolidated into the Plant Health (Great Britain) Order in 1987. Not until very late in December 1976 was there a harmonised EC regime to regulate trade for plant health purposes through the Plant Health Directive 77/93/EEC (Anon. 1977). The Directive was one of the most complex

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pieces of EC legislation, taking 19 years from first discussions and planning to its final implementation in May 1980 (Baker and Pemberton 1993). The 1976 system covered intra-community trade in plants and plant products and their imports from non-EU Member States (referred to as Third Countries). Amongst other things, 77/93/EEC listed those plants and plant products that were prohibited from entry into the Community and those requiring phytosanitary certificates, and pests whose introduction and spread within the Community was banned (Savage 1993). Third country material had to meet EC minimum standards but more stringent national standards were still permitted (Bartlett 1994). Thus plants traded across EU borders were still subject to checks at national customs posts, a practice inconsistent with the concept of a single market. Implementing a single EU market for plants required substantial legislative amendments to 77/93/EEC, described by Vereecke (1993). The amendments culminated in the creation of the single market for plants and plant products in 1993 whereby EU wide requirements for plant health became harmonized. Rather than plants and plant material being checked at national borders, EU producers wishing to market such goods in other Member States had to register with the NPPO. Official inspections of controlled material bound elsewhere in the EU would be made, and if the material met the plant health requirements it was issued with a “plant passport”. In England and Wales such duties were, and still are, performed by the Plant Health and Seeds Inspectorate (PHSI) (Ward 1993) which is now part of Fera. Not all plants or plant material are subject to such requirements. Instead it is usually restricted to plant propagating material such as cuttings, rootstocks, seedlings and young plants for planting, bulbs, corms and seed potatoes, and other selected material including wood and Citrus clementina fruit with leaves (Vereecke 1993). The removal of internal border controls between EU Member States means that once material has been cleared through an external border, it should be able to be moved without hindrance anywhere within the EC on the single market principle. As with all EC Directives, which are not self-executing, the amended 77/93/ EEC Directive laid down reforms needed in Member States’ domestic legislation. In the UK, Parliament implemented 77/ 93/EEC, as amended, through the Plant Health (Great Britain) Order 1993. The introduction of the single market forced a major shift in thinking about plant health from protecting national interests to protecting the wider European Community. Given the large number of amendments made, 77/93/EEC was consolidated into Council Directive 2000/29/EC of 8 May 2000 on protective measures against the introduction into the Community of organisms harmful to plants or plant products and against their spread within the Community, also known as the Plant Health Directive.

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There are weaknesses in the Plant Health Directive of a philosophical and historical nature. Philosophically, any plants not regulated by the Plant Health Directive are allowed entry into the EU with minimal regulation. Hence trades and pathways of which there is no prior experience develop with little scrutiny, posing plant health risks, and sometimes it is only after those risks are realised and new pests have become established that risk management measures are applied. Conversely risk management measures continue to be applied against some trades which have a long record of compliance and pose very low risk (e.g. apples from New Zealand and USA). When pests and plants were regulated by the original Directive 77/93/EEC, Europeans largely traded with former colonial partners. There was limited information about the pests of countries that have now emerged to be major trading nations, exporting increasingly large volumes of plants and plant products. Consequently the EU is now being confronted with progressively more pests from the Far East. However, any radical change to the current EU philosophy has the potential to create trade disputes within the WTO under the SPS agreement and is likely to be opposed by some trade interests within the EU. The European Commission drives European policy on plant health through its chairmanship of the Standing Committee on Plant Health (SCPH) that meets with NPPO representatives regularly through the year in Brussels (Bartlett 2000). That is not to say that the UK has a diminished role in determining national plant health policy. Indeed UK officials do influence the SCPH and can influence the development and revision of EU policy and legislation (e.g. MacLeod and Baker 1998; Sansford 1998; Bartlett 2000; MacLeod et al. 2002, 2005). Use of legislation is not the only mechanism available by government to protect UK plant health. Codes of Practice such as the “Plant health code of practice for the management of agricultural and horticultural waste” (MAFF 1998; Defra 2008b) and “Horticultural code of practice: Helping to prevent the spread of invasive nonnative species” (Defra 2005) have been developed with industry sectors. Undertaking wide consultation and through joint working with stakeholders in developing such codes of practice, leads to a greater acceptance of change (Ashby et al. 2005) which, through rigid legal enforcement, may otherwise be more challenging.

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public trust in government management and administration of outbreaks (Scott et al. 2004). Using narrow sciencecentred decision-making approaches has resulted in high profile failures and ‘crises’ of public legitimacy, confidence and trust (Woods 2005). In the light of high profile breakdowns in public confidence over animal health issues impacting on human health, van Zwanenburg and Millstone (2005) have called for a reorganization of science-based risk policy-making. By viewing rural areas through an agricultural lens, government failed to appreciate the presence of other communities and stakeholders that may be affected in the countryside (e.g. those involved in rural tourism and related sectors). Attempts to combat Foot and Mouth Disease caused major unforeseen economic impacts because not all receptor communities and stakeholders were identified (Donaldson et al. 2002). Some recent commentators question the pre-eminence of scientific experts when it comes to environmental decision-making (e.g. Irwin 1995; Bryant and Wilson 1998). They have argued that environmental decision making has to be grounded on partnerships between experts, policy advisers and stakeholders, and that more inclusive or participatory approaches are needed to ensure that account is taken of other types of knowledge, beyond that associated with the scientific and technical realm (e.g. Burgess et al. 1998; Irwin 2001; Kapoor 2001; Kates et al. 2001; O’Riordan 2000; Wilson and Bryant 1997). Some commentators argue that new types of scientific dialogue are emerging, which they refer to variously as ‘sustainability science’ (Kates et al. 2001; Moll and Zander 2006) “citizen science” and “post-normal science” (Nowotny et al. 2001; Potschin and Haines-Young 2006). Figure 2 suggests a framework in which much applied science, or at least that applied science which seeks to inform or support policy, is now set. Future legislation and management of the risks presented by non-native plant pests may have to take account of such attitudes and continue to build stakeholder consultations into protocols for decision making. There is now widespread acknowledgement that while evidence-based policy must be based

More inclusive decision making Traditionally, in science-led government departments and ministries dealing with agriculture, food and the environment, decision-making has resulted from the interaction of scientists and policy advisors. However, significant unanticipated effects of disease outbreaks can result in loss of

Fig. 2 Developing environmental policies—key players and their interaction

Evolution of the international regulation of plant pests

on the best science, it must also take account of wider social and economic contexts in which that knowledge is set and used (Anon. 2006). The importance of citizen science in the issue of invasive diseases has been recognised by Crowl et al. (2008). However, plant pests and plant health have a relatively low public profile compared with animal pests and diseases and engaging the public over plant health matters will remain a challenge whilst public awareness is low. Just as in the UK, other European nations recognise that agriculture has a multifunctional role, e.g. it covers various policy objectives, such as the maintenance of food supply, has the ability to supply non-market public goods especially with respect to the environment (positive externalities), and maintains the viability of rural areas (FAO 2001). Norway specifically values agriculture in that it also can help preserve cultural heritage (WTO 1999). For these reasons, environmental decision making, including plant health policy decision-making, has to engage with a broader community of users than those traditionally consulted. Although the EC has consulted interested parties during policy development in the past, up until 2002 there was no standard Commission-wide approach on how to undertake consultations. In December 2002 the Commission adopted a number of principles that should govern its relations with stakeholders and a set of minimum standards for the Commission’s consultation processes. Subsequently the Commission contracted independent consultants to work with stakeholders in order to evaluate the European legislation governing the marketing of seeds and plant propagating material within the European Union (FCEC 2008). An example at the national level is seen in the UK where government has adopted a policy of more transparent consultation. The Better Regulation Executive, part of the Department for Business, Enterprise and Regulatory Reform, aims to work with regulators and other government departments to change attitudes and approaches to regulation, to become more risk-based, and to improve the ways in which new regulations are communicated.

Regional context: wider European cooperation European and Mediterranean Plant Protection Organization Some plant pests have been found to spread significantly during periods of war and social upheaval (FAO 2001). In Europe, Colorado beetle spread significantly during WWII (Bartlett 1979). At a meeting in Paris in April 1951, officials from 15 governments met and agreed to combine the responsibilities of the International Committee for the Control of Colorado Beetle with the activities of the European Working Party on Infestation Control, that

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worked on pests of stored foods and rodent pests of crops, thereby forming The European and Mediterranean Plant Protection Organization (EPPO) (EPPO 1951; Smith 1979). The first specific pests to be given special attention by EPPO were Colorado beetle (L. decemlineata), potato root eelworm (Heterodera rostochiensis), San Jose scale (Diaspidiotus (as Aspidiotus) perniciosus) and potato wart disease (caused by Synchytrium endobioticum). More generally “insect, fungus and rodent pests of stored foods, and rodent pests of crops” were also within the scope of EPPO work. EPPO has its headquarters in Paris and since 1951 EPPO membership has grown from 15 countries to 50 (Table 3). Over the same period the number of plant pests EPPO has an active interest in has grown to over 330. Today EPPO aims to develop an international strategy against the introduction and spread of pests that damage cultivated and wild plants in natural and agricultural ecosystems (Petter et al. 2010); encourage harmonization of phytosanitary regulations and all other areas of official plant protection action; promote the use of modern, safe, and effective pest control methods; and, provide a documentation service on plant protection. Through such aims, EPPO can inform and facilitate collaboration in support of the role of NPPOs in the European and Mediterranean region with regard to the technical justification of phytosanitary measures, sustainable and effective plant protection practices and scientifically-based harmonization of phytosanitary methods and procedures. EPPO achieves its aims by setting regional standards for phytosanitary measures and plant protection products, recommending pests for regulation, organizing specialist meetings bringing together experts from all parts of the EPPO region, participating in global activities related to phytosanitary measures coordinated by the IPPC Secretariat within FAO, organizing international conferences and workshops for plant protection researchers and practitioners, publishing the journal EPPO Bulletin, providing an electronic documentation service through the EPPO Reporting Service and distributing database systems. EPPO is one of ten Regional Plant Protection Organizations (Table 2). Membership of each RPPO is shown in Table 3. Collectively, the RPPOs recommend that over 1,000 pests be regulated (EPPO 2007). RPPOs work with the IPPC suggesting subjects around which ISPMs can be developed, identifying regional experts to help draft standards and organizing consultations on outputs. It must be recognized that EPPO does not regulate pests, rather it makes recommendations about which pests to regulate. Whilst EPPO and the EU authorities have worked together to harmonize lists of quarantine pests, the speed of regulatory decision making within the EC is a weakness within the European plant health regime, e.g. the polyphagous white fringed weevil Naupactus leucoloma, a pest of many field vegetable crops that has spread from South America into South Africa, Australia, New Zealand and the

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Table 2 Regional plant protection organizations Abbreviation

Full name

Geographic region covered

Approximate number of pests recommended for regulationa

APPPC CAN COSAVE CPPC EPPO IAPSC NAPPO NEPPO OIRSA PPPO

Asia and Pacific Plant Protection Commission Comunidad Andina Comité regional de sanidad vegetal para el Cono Sur Caribbean Plant Protection Commission European and Mediterranean Plant Protection Organization Interafrican Phytosanitary Council North American Plant Protection Organization Near East Plant Protection Organization Organismo internacional regional de sanidad agropecuaria Pacific Plant Protection Organisation

Asia and Pacific South America I South America II Caribbean Europe and Mediterranean Africa North America Middle East Central America Pacific

254 77 147 419 337 137 (403)b 23 250 147

a

A-S. Roy, EPPO Secretariat, Paris pers. comm

b

NAPPO does not publish a list of pests recommended for regulation, however the pests regulated by the USA are used here as a proxy. Approximately 403 pests appear on the USDA APHIS regulated pest list (USDA 2000)

USA, was first recommended by EPPO for regulation in 1998 but not added to EC legislation until 2004. Unfortunately the lack of rapid decision making can allow pests to arrive, establish and spread before sufficient measures are in place to inhibit their arrival, making eradication less likely. For example, the South American tomato moth, Tuta absoluta, was first recommended by EPPO for regulation in 2004 at a time when it was not present in any European or EPPO country. However, it was not added to EC legislation. Outbreaks of the pest occurred on tomatoes in Spain in 2007 and by 2009 it had spread and outbreaks were reported in France, Italy, Malta, the Netherlands, Portugal, Switzerland and UK (EPPO 2009). Any attempt to eradicate T. absoluta within Europe will now be prohibitively expensive.

public confidence EFSA stresses that it operates in a very transparent manner and that it is independent of risk management decision makers, e.g. independent from the European Commission. Due to their mutual interest in pest risk assessment and the evaluation of risk management measures, EFSA and EPPO have taken steps to recognise and acknowledge their respective roles and senior staff from EPPO and EFSA have met and an agreement to avoid duplication of effort, while still maintaining EFSA independence, is planned.

European Food Safety Authority

The drivers responsible for the continued international spread of plant pests will not easily be halted. Brasier (2008) calls for a substantial reduction in the international trade of plants as the best means of reducing threats from pests moving to new geographic regions. Whilst this would without doubt reduce pest spread, it is very unlikely that trade will be significantly reduced in the near future. In a similar vein, a more measured output from the Conference of the Parties to the CBD, was the invitation to the WTO Committee on Trade and the Environment to consider the effects of the spread of invasive species when assessing the impacts of further trade liberalization (CBD 2002), although this was also in relation to climate change (CBD 2002). Pests also spread as a consequence of war or conflict. Civil unrest has permitted many introduced pests to spread rapidly. Factors contributing to pest spread in conflict zones include the lack of border controls and the increased

Following a series of events where the public lost confidence in aspects of food safety in Europe in the late 1990s (e.g. Vos 2000; Pennington 2003), the European Food Safety Authority (EFSA) was established in January 2002 to act as an independent source of scientific advice and to communicate risks associated with the food chain. The remit within EFSA’s founding regulation (EC 178/2002) covered food and feed safety, nutrition, animal health and welfare, plant protection and plant health. EFSA produces scientific opinions and advice on subjects within its remit to inform European policies and legislation through the work of its various scientific panels. Panel members are drawn from experts across Europe. The EFSA Panel on Plant Health (PLPH), first formed in 2006, specifically aims to help decision making with respect to the risk posed by pests that cause harm to plants, plant products or biodiversity. To rebuild

Future challenges to plant health Drivers of pest spread

Evolution of the international regulation of plant pests

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Table 3 Country membership of each regional plant protection organization

Table 3 (continued)

Member states of APPPC

Member states of PPPO

Member states of NEPPOa

Dominica

Belgium

Dominican Republic

Bosnia and Herzegovina Cameroon

Australia

American Samoa

Algeria

French Guiana

Bulgaria

Cape Verde

Bangladesh

Australia

Egypt

Grenada

Croatia

Central African Republic

Cambodia

Cook Islands

Jordan

Guadeloupe

Cyprus

Chad

China

Fiji

Libya

Guyana

Czech Republic

Comoros

Fiji

France

Malta

Haiti

Denmark

Cote d’Ivoire Dem. Rep. of Congo

Burundi

French Polynesia

French Polynesia

Mauritania

Jamaica

Estonia

India

Guam

Morocco

Martinique

Finland

Djibouti

Indonesia

Kiribati

Pakistan

Mexico

France

Egypt

Korea Dem. People’s Republic Korea, Republic

Marshall Islands

Sudan

Netherlands Antilles

Germany

Equatorial Guinea

Nicaragua

Greece

Eritrea

Micronesia

Syria

Panama

Guernsey

Ethiopia

Laos

Nauru

Tunisia

Puerto Rico

Hungary

Gabon

Malaysia Myanmar

New Caledonia New Zealand

Yemen

Saint Lucia

Ireland

Gambia

Nepal

Niue

New Zealand

Northern Mariana Islands

St Kitts-Nevis

Israel

Ghana

Suriname

Italy

Guinea

Trinidad and Tobago

Jersey

Guinea-Bissau

Palau

Turks and Caicos Islands Jordan

Kenya

Papua New Guinea

Papua New Guinea

Venezuela

Lesotho

Philippines

Pitcairn

Virgin Islands (British)

Kyrgyzstan

Liberia

Solomon Islands

Samoa

Virgin Islands (US)

Latvia

Libya

Sri Lanka

Solomon Islands

Lithuania

Madagascar

Thailand

Tokelau

Luxembourg

Malawi

Tonga

Tonga

Macedonia

Mali

Viet Nam

Tuvalu

Malta

Mauritania

Western Samoa

United States of America

Moldova

Mauritius

Morocco

Mozambique

Vanuatu

Netherlands

Niger

Wallis and Futuna Islands

Norway

Nigeria

Poland

Republic of Congo

Portugal

Rwanda

Pakistan

Member states of NAPPO Canada

Member states of COSAVE Argentina

Member states of OIRSA Belize

Mexico

Bolivia

Costa Rica

United States of America

Brazil

Dominican Republic

Chile Paraguay Uruguay

El Salvador Guatemala Honduras Mexico Nicaragua Panama

Member states of CAN Bolivia Colombia Ecuador

Kazakhstan

Romania

Sao Tome and Principe

Russia

Senegal

Serbia

Seychelles

Slovakia

Sierra Leone

Slovenia

Somalia

Spain

South Africa

Sweden

Sudan

Switzerland

Swaziland

Tunisia

Tanzania

Turkey

Togo

Ukraine

Tunisia

United Kingdom

Uganda

Uzbekistan

Zambia Zimbabwe

Peru Member states of CPPC

Member states of EPPO

Member states of IAPSC

Aruba

Albania

Algeria

Barbados

Algeria

Angola

Colombia

Austria

Benin

Costa Rica

Azerbaijan

Botswana

Cuba

Belarus

Burkina Faso

IPPC Website. https://www.ippc.int/index.php?id=13310&L=0 a

NEPPO is the newest RPPO. The agreement for the creation of NEPPO was signed in 1993 and entered into force on 8 January 2009 with 12 countries having deposited their ratification or accession with FAO (http://www.fao.org/legal/treaties/024S-E.HTM)

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unregulated movement of military personnel, equipment and supplies, such as emergency food aid carrying pests from outside the conflict zone. Bartlett (1993) discussed the European example of L. decemlineata during WWII and predicted that the Yugoslav/Balkans war of the 1990s may also have increased phytosanitary risk, which has since been evidenced by the introduction and rapid spread of Diabrotica virgifera virgifera (EPPO 2008). It has been suggested that D. virgifera virgifera was first introduced in 1990 by military air transport from North America (EPPO 1996). Bioterrorism Although use of plant pests by criminals or terrorists is rare (Zilinskas et al. 2004) their use could spread pests more widely and new sources of potential threat have been identified through assessment of the use of pests for bioterrorism (Madden and Wheelis 2003). Plant pests can be used as weapons and be deliberately introduced to reduce food security or have a more indirect impact on a nations’ economy e.g. by denying access to lucrative export markets. Developing plans for emergency preparedness has enabled scientists to obtain substantial funds from US government sources (Madden and Wheelis 2003; Meyerson and Reaser 2003). In developing procedures to counter such threats, spin-off benefits are to be expected for more conventional plant pathologists and future prevention and management systems will be strongly influenced by new technology and the growing role of the private sector (Waage and Mumford 2008). Climate change Now that the weight of scientific evidence about the causes of climate change has been widely accepted (IPCC 2007; Nielsen-Gammon 2007), and it is recognised that climate change can facilitate the spread and local severity of pests (Cannon 1998; Baker et al. 1998; Baker et al. 2003; Scherm 2004; Simberloff 2006; Sutherst et al. 2007; Sutherland et al. 2008; Ghini et al. 2008), pests can be expected to continue to change their distribution as changes in ecological conditions associated with climate change increase the susceptibility of hosts in new areas. It is also legitimate to consider reviewing existing risk analyses that formed the basis of trade-permitting or trade-restricting decisions (Committee on World Food Security 2005). However, whilst climate change can cause pests to expand their ranges, a pests’ impact at the margin of its distribution may well be lower than its impact at the core of its distribution (e.g. Zocca et al. 2008). It will therefore be important to assess the impact of climate change on potential pests on a case by case basis.

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Institutional challenges: implementation of standards Shine (2007) noted that a technical review of the international regulatory framework designed to prevent the spread of invasive alien species, which can include plant pests, did not reveal any inadequacies but instead found problems with inadequate implementation. Implementation can be hampered nationally when government departments have different and conflicting goals, e.g. departments of agriculture or trade that have a primary interest in production, versus departments responsible for conservation. Internationally issues of concern include the lack of coordination between neighbouring countries, regional free trade agreements which relax or remove border controls, low public awareness, few deterrents to those that introduce risk agents, and constraints on funding giving rise to a lack of resources to operate comprehensive quarantine and risk assessment systems. Recognising that the threat from nonnative pests is persistent and of global relevance, international cooperation and policies that support efforts to mitigate the risks are essential. Developing good governance Around the world today in many developing and transition countries, establishing appropriate plant health legislation, and having an official system to control its quality and reliability, is a major challenge (Vallat and Mallet 2006). As a result many countries have no effective NPPO. The major infrastructure required by a country to develop an effective NPPO can be determined through use of the FAO phytosanitary capacity evaluation tool (ICPM 2004). Improved international cooperation is noted as being a key way to deal with global threats such as food security (Epstein 1997). The interdependence of countries required to tackle pests leads developed nations to support developing countries in improving capacity to deliver such services. For example Australia and New Zealand place a high priority in helping build sanitary and phytosanitary capacity in neighbouring ASEAN countries, and this provides Australia and New Zealand with opportunities to take action offshore to mitigate threats posed by exotic pests (Anon. 2008). Countries that have acceded to the EU since 2004 have taken part in “twinning projects” where they partner a more established Member State in order to develop their plant health regime and harmonise it with EC requirements. In preparation for further expansion of the EU, the Food and Veterinary Office (FVO) evaluates the phytosanitary capabilities of each candidate country and the EU Technical Assistance Information Exchange Unit (TAIEX) facilitates assistance for these and pre-accession countries.3 It will 3

TAIEX website: http://taiex.ec.europa.eu/.

Evolution of the international regulation of plant pests

require major investment to improve plant health and border controls for countries such as Turkey (Schmidt 2006). In addition to issues of plant health risk management, plant commodities that are foods have additional food safety controls to comply with. Food safety regulations can have a major impact on food security. An historical review of the development of food safety legislation is beyond the scope of this study, other than to note that in addition to legislative requirements, private interests are key drivers of food supply chains and they have led to the institutionalisation of standards-setting and quality requirements (Barling 2007). The European Commission has recognised the interdependence of food safety, animal feed and plant health by organising them within a single Directorate General—SANCO (Santé et Consommateurs), including having a combined inspectorate, the FVO. Challenges in Africa To improve the management of risk in plant health and contribute to better food security in Africa, efforts to develop systems of “open quarantine”, allowing international exchange of disease resistant varieties of plant material, have been made. Implicit in the term open quarantine is the setting of phytosanitary protocols that do not require plant confinement in structures such as secure glasshouses or screenhouses during a period of quarantine. Such a system was viewed as appropriate for Africa where the need to introduce new plant varieties is strong but where quarantine infrastructure in many countries is weak. The technique was initially used successfully in East and Central Africa (Mohamed 2003; Danson et al. 2006) with the international exchange of high quality cassava material resistant to African cassava mosaic virus, used to alleviate impacts of the devastating cassava mosaic disease outbreaks of the early 1990s. However, since late 2004 Cassava brown streak virus (CBSV) has been spreading in East Africa via infected propagating material and to a lesser extent by Bemisia tabaci, a whitefly vector. CBSV can be a devastating pest responsible for loss of cassava root quality and yield but it is difficult to detect since foliar symptoms are not conspicuous. Due to the limited diagnostic capability to identify CBSV within quarantine stations there was a call for the restriction of movement of cassava cuttings through the open quarantine system (Ntawuruhunga and Legg 2007). Individually many African countries do not have the capacity to provide technical plant health services (Smith et al. 2008) or comply with international phytosanitary standards and are consequently excluded from lucrative export markets. Lack of capacity also inhibits a nation’s ability to deal with invasive pests potentially threatening local food security. To address some of these issues, East and South African countries are co-operating to

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establish a regional Centre of Phytosanitary Excellence (CoPE) based in Nairobi, Kenya. The CoPE aims to establish a phytosanitary information management system and build a plant inspection facility, both as a demonstration and training resource. Some infrastructure changes will be required to set up the legal and institutional framework within which the CoPE will operate (Otieno 2008). Detection and monitoring Even with ISPMs adequately implemented, as the four Ts mentioned previously continue to grow, each will continue to present challenges for regulators and especially put pressure on border inspections. A study comparing those species that were intercepted by phytosanitary services in Austria and Switzerland between 1995 and 2004, with species that established over the same period showed that only 10% of species that established were ever intercepted (Kenis et al. 2007), evidence that better targeting of pathways to detect incursions are needed. There has been much work on network epidemiology that suggests that if the number of business to business links varies greatly between individual businesses, then targeting control towards super-connected traders may be a more effective way to reduce the risk of introduction of new pests than a slightly increased control of all potential pathways (Jeger et al. 2007; Harwood et al. 2009; Moslonka-Lefebvre et al. 2009). It is not only imports that are important in spreading non-native pests. Movement of plants within a single country can have impacts for plant health, as illustrated by the spread of P. ramorum through US and UK nurseries (Stokstad 2004; Xu et al., 2009). Equally a plant health campaign against a pest can be inhibited if the pest develops resistance to a particular treatment. For example, in New York State Erwinia amylovora was reported as being resistant to streptomycin following movement of plants from Wisconsin (Russo et al. 2008). Development of nation-wide monitoring systems (e.g. Delos et al. 2007; Tkacz et al. 2008), can provide early indications of emerging pests and, if maintained consistently through time, could also provide much needed long-term data, in relation to the impact of pests and of climate change. Longterm datasets, where they exist, are invaluable in predicting threats to plant health from global factors, including climate change (Jeger and Pautasso 2008). Nationwide monitoring schemes are now common for biodiversity, and there are great benefits to be gained if pests were to be included in these surveys (Desprez-Loustau et al. 2010). However, the general shortage of taxonomists, recognised as the “taxonomic impediment” (Hoagland 1996) could constrain the development and potential benefits of such surveys, for example, by allowing invasive pests to remain undiagnosed and hence lose opportunities for appropriate interventions.

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Weight of evidence Baker and MacLeod (2005) recognised that lack of data presented significant and ongoing challenges to those charged with assessing the risk of non-native pests. Precautionary action has often been used in public health where the public receive the benefit of the doubt. However, the application of such an approach to environmental hazards only emerged the end of the 20th Century (EEA 2001). Identifying when there is sufficient evidence in order to regulate a pest has, and will continue to be, a major difficulty. However, waiting until there is conclusive evidence before making a decision to regulate a pest is likely to lead to the pest becoming more costly to manage since it is likely to spread whilst evidence is being collected.

Conclusions Plant pests have always threatened food security and as our understanding of pests began to develop, so too did the regulatory systems to control them. The present international model for plant protection was founded at a time when the primary focus was on protecting crops. There were fewer trading nations, transport was slower and there was less diversity in the range of plants and commodities traded. Whilst perhaps more appropriate in earlier times, current plant health regimes face the constant challenge of preventing pest spread whilst operating within agreements and following guidelines that can be slow to change and difficult to implement. Developing nations, not burdened by established systems, that have recently begun to build their own plant protection regimes would benefit from sharing resources and cooperating with neighbouring countries. Closer coordination of activities between NPPOs facilitated by RPPOs would help at a regional level. EPPO, as the oldest RPPO, provides a good model for less experienced RPPOs. Rather than follow rigid European regulations (MacLeod 2007), the UK and some other EU Member States have traditionally supported a more independent attitude to plant health (Baker and Pemberton 1993). However, there is no denying that European interests have a major influence on UK plant health work (Bartlett 1994, 2000). As a ‘weakestlink’ public good (the plant health status of the EU as a whole can only be as good as that of the weakest Member State) it is imperative that Europe continues its long history of collaboration and major involvement in developing plant health internationally by being increasingly active on a global scale. However, in future, Europe’s international influence may decline as the influence from non-European countries such as Brazil, Russia, India, China and parts of Africa increases.

A. MacLeod et al.

It is clear that when moving plants and plant products internationally no supply system can ever be totally secure. Plant health and food security is about managing the pest risks associated with such movements. Identifying, assessing, managing and mitigating risk has, in recent years, become a much more conscious exercise in the public and private sectors (Defra 2006) and regulatory scientists have made efforts to explain their role and reach out to a wider research community (e.g. Magarey et al. 2009; Rodoni 2009). If this can facilitate collaborative research to better identify and predict pathways of entry, pest impacts and appropriate risk management measures, then progress will have been made. In the 21st Century plant health is not only about ensuring food security but also concerns protecting growers or the environment from burdens on their well-being. In the UK and elsewhere, following the outbreak of Foot and Mouth Disease in 2001, politicians have a greater awareness of the significance of multi-functional agriculture, which not only provides food commodities but also manages the countryside, preserving wildlife for the benefit of the wider public. Increasingly, the need to involve stakeholders in the decision making process is regarded as essential (Lawton 2007). Drawing upon a wider knowledge base, by assessing risks in a more interdisciplinary fashion and including stakeholders from an early stage, regulations and actions should become more sustainable (Anon. 2005). Acknowledgements This paper derives from the RELU funded project “Growing Risk? The potential impact of plant disease on land use and the UK rural economy”. Collaborating partners are: the University of Warwick, Imperial College, University of Gloucestershire and the Food and Environment Research Agency. Richard Baker, Paul Bartlett, Lesley Cree, Andrew Gaunt, Wyn Grant, Mike Ormsby, Françoise Petter, Peter Reed and Martin Ward provided useful comments on earlier drafts. Thanks are also due to three anonymous referees for their comments on the manuscript.

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Alan MacLeod is a pest risk analyst at The Food and Environment Research Agency. He has worked to assess the risk to plants in the UK, EU and EPPO from pests of actual or potential quarantine significance since 1995. Alan is a member of the EPPO Panel for Development of Pest Risk Analysis (PRA) and a core member of the EPPO Expert Working Group for Performing PRA as well as being a Member of the Society of Risk Analysis. He is Chairman of the International Advisory Group for PRA through which he has been working with PRA specialists from around the world on development and delivery of PRA training workshops, delivering such training in Asia and Africa.

Mike Jeger is Professor of Plant Epidemiology in the Division of Biology, Imperial College London, based at the Silwood Park campus. He was previously based at the Wye campus of Imperial College, before it closed in 2007. He received a PhD from the University College of Wales, Aberystwyth in 1978 and subsequently worked at East Malling Research Station, Texas A&M University, the Natural Resources Institute, and Wageningen University in the Netherlands, before moving to Wye in 1999. Throughout his career he has carried out research on diseases of a wide range of temperate and tropical crops with an emphasis on epidemiology and mathematical modelling, most recently of plant viruses and the risks posed by new invasive pathogens such as Phytophthora ramorum in the UK nursery trade. Professionally he has served as President of the British Society of Plant Pathology (1999), and is currently President of the Association of Applied Biologists and Editor-in-Chief of the European Journal of Plant Pathology.

Marco Pautasso is a scientist interested in network epidemiology, landscape pathology, conservation biogeography and peer review. He has contributed to literature reviews on global change and plant health, the biodiversity of wood-decaying fungi, geographical genetics, the conservation of forest trees and peer reviewing interdisciplinary papers. Research has dealt with epidemic development in small-size directed networks, the scale-dependence of the spatial correlation between human population and biodiversity, geographical patterns of the species richness of the living collections of the world’s botanic gardens and peer review delay and selectivity in ecology journals.

Roy Haines-Young is Professor in Environmental Management and Director of the Centre for Environmental Management (CEM) in the School of Geography, University of Nottingham, and formerly led the Environmental Science and Policy Group (ESPG) within the Centre for Ecology and Hydrology (CEH). Although trained as a natural scientist, he has sought to develop a stronger social content in his recent work. He has worked extensively with the policy makers in Central Government and it agencies, and recognises the need to develop a science that is responsive to the wider public debates about environmental issues. He is adviser for environmental issues to research councils, but also Governmental Agencies.