Protecting Australia’s plant health: plant quarantine in an evolving biosecurity system†
Mark Whattam A , Stacey Azzopardi A * , David Nehl A , Aaron Maxwell A and Kevin Davis AA
Abstract
As a geographically isolated and island continent, Australia has historically been protected from the impact of many damaging plant pests found overseas. However, the advent of modern transport systems and greater global trade in live plants, seed and plant products is increasing the movement of pests including invertebrates, pathogens, and weeds. Exclusion of these threats through an effective biosecurity system is essential to support and protect Australia’s agricultural producers and unique flora. Biosecurity measures must balance risk-based regulation with successful trade of goods, including live plants, seed and plant products. Although achievement of zero biosecurity risk is not a broadly practical outcome, geographic exclusion of threats is an effective approach to support and protect Australia’s unique environment. This is particularly important in the trade of live plants as nursery stock. Latent infection presents a significant hurdle for detection of plant pathogens in border inspections to exclude their entry with imported plants. Post-entry plant quarantine enables latent infection to be expressed as visible symptoms, while providing sufficient time for targeted testing of asymptomatic plants. Here we provide a synopsis of the pivotal role plant quarantine has and continues to play in Australia’s biosecurity system.
Keywords: agriculture, biosecurity, diagnostics, diseases, environment, historical article, plant health, plants, post-entry quarantine, quarantine.
Introduction
Globally, the ecological and economic impact of plant pests including invertebrates, weeds, and microorganisms on plant health is staggering. The Food and Agriculture Organization (FAO)1 estimates that pests annually destroy or impact 40% of all crops produced worldwide with plant diseases costing the global economy over $220 billion and invasive insects at least $70 billion. Consequently, pragmatic and effective regulations that prevent or minimise the entry and establishment of plant pests to new locations are extremely important for the protection of a country’s economic, environmental and social well-being.
This article reviews the evolution of Australia’s longstanding, effective plant biosecurity system that is the envy of many countries. Australia’s biosecurity system protects agriculture, forestry, and fishery export industries worth $86.8 billion, a tourism sector worth $50 billion, environmental assets worth more than $5.7 trillion and more than 1.6 million jobs.2 Approximately 70% of Australia’s agricultural produce is exported, providing a reliable source of food and fibre to our trading partners. Australia’s freedom from many of the world’s most serious plant pests allows greater access to markets and premium prices. This favourable status must be maintained.
Not only do Australians depend on fresh food, clean drinking water, and productive agricultural trade for a prosperous society, it is our duty as custodians of the lands in which we live to care for our environment through our ongoing connection to Country, upholding the culture and values of Aboriginal and Torres Strait Islander peoples and our wider community. All this, providing us with the way of life we value so much, will be at risk if we fail to maintain a strong focus on biosecurity and managing potential threats.
Historically, Australia’s island status and geographic isolation have played an important role in reducing the entry of many exotic and damaging pests. However, the advent of modern shipping and air freight combined with the liberalisation of international trade has resulted in large-scale global movement of people and cargo including plants and plant products providing ready pathways for rapid, long-distance movement of many plant pests. There is a widely recognised correlation between the level of trade and transport and alien pest invasion.3 Increasing invasion rates are documented for plant movement into North America4 and Europe.5 Annually, over 18,000 vessels, 1.8 million sea cargo consignments, 41 million air cargo consignments, 152 million international mail items and more than 18 million passengers arrive in Australia, and numbers are growing every year. Between 2012 and 2018, more than 1.9 million items of biosecurity concern were seised at airports. During the same period, more than 104,000 pests in air cargo and 35,800 pests in sea cargo were identified, with approximately 0.6 per cent being high-priority exotic plant pests.6 This shift in trade volume has placed pressure on biosecurity resources and, in Australia this is being addressed across all stages of the biosecurity continuum—pre-border, at the border and post-border.
Detection of invertebrates and seeds of invasive plants is generally achieved through direct observation of organisms, as well as signs and symptoms of infestation or infection, and this method is applied both pre-border through offshore certification programs and at the border, in mandatory biosecurity inspections. In contrast, the primary step in screening for plant pathogens post-border has historically been dependant on the observation of disease symptoms, allowing for potential failure to detect asymptomatic or latent infections. Post-entry quarantine (PEQ) has played a pivotal role in allowing the safe and timely entry of nursery stock imported from overseas. PEQ is an effective mechanism for allowing latent infections to be expressed as visible symptoms, while allowing sufficient time for testing asymptomatic plants for high-risk pathogens. Here we provide a synopsis of the role plant quarantine plays in Australia’s biosecurity system in protecting plant industries and the environment from exotic plant pathogens.
The act of quarantine
The word ‘quarantine’ derives from the Italian term quaranta giorni that translates to ‘space of forty days’. This number has proven its value historically. An isolation period of forty days was applied to ships and their travellers across Europe, as a period of detention when moving from affected countries during the bubonic plague, or Black Death in the years following 1347.7 Quarantine, as physical separation, has been enforced to minimise contact between infected and non-infected people or goods or at least allow time for those that were infected, to develop symptoms while in isolation.
The earliest documented phytosanitary legislation was enacted in Rouen, France in 1660. A new law directed landholders to destroy barberry (Berberis vulgaris) to protect wheat crops from black stem rust caused by the fungus Puccinia graminis.8 The first international phytosanitary agreement was the ‘International Convention on Measures to be taken against Phylloxera vastatrix’, that was signed by seven European countries in September 1868.9 This grapevine root feeding aphid was introduced into Europe in 1862. The Convention outlined several measures that still form the basis of many phytosanitary agreements today. These included: providing written assurance of the Phylloxera-free status of host material; powers to inspect and destroy infested material; and signatories to establish an official body to administer and implement the measures.
Prior to federation, quarantine in Australia was primarily focused on human and animal health. In October 1803, the third Governor of New South Wales, Philip King deemed it ‘expedient to declare all vessels cleared from New York to perform a period of fourteen days quarantine to manage the risk of the plague entering the colony’.10 The first quarantine order relating to agriculture was the Cattle Disease Regulation Act 1861 (New South Wales), introduced to regulate the importation of cattle into the colony to prevent the introduction of contagious or infectious disorders.11 A ‘carrot and stick’ approached was adopted. Farmers who breached this quarantine order had their cattle confiscated and hefty fines of £10–50 were imposed. Conversely, compensation was paid to farmers who legally declared imported cattle but had their cattle destroyed by the authorities because of fears of disease.12 Also in the early 1860s, sheep scab emerged as a serious threat to the wool industry, and various disease containment measures were introduced, such as the appointment of sheep scab inspectors, and the imposition of fines for any farmer who failed to control the disease.13 In 1868, various states introduced quarantine controls at their borders to manage the risk of sheep scab entering from Victoria.14 Even back then, there were mixed views on the benefits of introducing genetically superior sheep for breeding purposes compared with the risks of introducing new diseases.15
Mirroring the experience in Europe, some of the first plant quarantine regulations in Australia were introduced to allay the concerns of wine grape growers. On 23 December 1867, an Act to Prohibit the Importation of Grape-vines, Grape-vine Cuttings, and Grapes was enacted by the New South Government to prevent the introduction of grapevine powdery mildew caused by the fungus Erysiphe necator, a pathogen that was devastating grape vines in Europe and had become prevalent in Queensland.16 Alas the Act failed to prevent the introduction of powdery mildew into New South Wales and it lapsed on 1 January 1870. This Act was reintroduced on 5 November 1878 to prevent the introduction of phylloxera.17 The Vine Diseases Act 1886 (New South Wales) gave the governor a range of powers to prohibit the importation of vines, to appoint inspectors of vineyards who had the right of entry onto any property, and to order the destruction of a vineyard.18
Substantial new plant quarantine legislation was introduced in the 1890s, including The Vegetation Disease Act 1895,19 that allowed the Victorian Government to prohibit the entry of trees, plants or vegetables into the colony or from another part of the colony, and to allow government officials to inspect and destroy diseased plants. Similar legislation was introduced across Australia over the next few years. Orchardists were the primary motivators for these new laws, because they were worried about the spread of insect and other pests such as the codling moth, fruit fly, slugs and scale insects.
The Conference of Ministers of Agriculture was convened for the first time on 28 May 1898 in Brisbane, and attended by the ministers from Victoria, New South Wales, and Queensland.20 While the problem of cattle tick dominated the proceedings, plant health was discussed, and it was decided to introduce uniform legislation in the different colonies to prevent the importation of plant diseases. Ironically, all the resolutions related to insect pests and not a single plant pathogen was mentioned. In summary, the resolutions of the meeting were to (1) establish a system of plant health certification for the export of fresh fruit, by declaring that the fruit has been treated with an appropriate insecticide for example; (2) require that imported plants are inspected and disinfested if necessary by an authorised government official; and (3) develop a list of high priority pest threats to be dealt with by the relevant Acts in the different colonies.
In Australia, national plant quarantine regulations first came into operation on 1 July 1909 following the passing of the Quarantine Act 1908 (Commonwealth). The Act provided for a change in ownership of the quarantine stations from the states to the Australian government. Other provisions of the Act were that ‘the Governor-General may, by proclamation’ declare any port in Australia to be the first port of entry for overseas vessels; to appoint officers for quarantine duties; to direct what particular plants or animals may be landed; to prohibit the introduction of any noxious insect pest, disease, germ, microbes, any disease agent, culture, virus, or substance. It will direct the importation of any animal or plant to be prohibited if it is believed there is danger likely to arise from their introduction. Power will be given to declare any part of Australia a quarantine area, in which any quarantinable disease or pests affecting animals or plants exist. Oversea vessels, unless specially exempt, will be subject to quarantine, and all animals or plants imported will be required to undergo examination, the importer to stand any expense incurred.21
When the Quarantine Act was passed, sea travel was the only way people and goods could reach Australia. The main concerns were animal and human diseases, such as the bubonic plague, yellow fever, smallpox, cholera, and leprosy. Throughout the twentieth century the Quarantine Act underwent many amendments to reflect the changes associated with plant pest risks and modernised transport pathways.
Our evolving plant quarantine story
The Quarantine Act was administered by the Commonwealth Department of Trade and Customs until 1921 when responsibility was transferred to a newly formed Department of Health created after the worldwide influenza epidemic following World War 1.
In 1984, the policy and administration of animal and plant quarantine aspects of the Quarantine Act were transferred from the Department of Health to the Department of Primary Industries (now the Department of Agriculture, Fisheries and Forestry; ‘the department’).
Australia’s biosecurity system has been subject to several reviews, each having an impact on the delivery of services. In 1988, the Lindsay review recommended retaining the existing state quarantine services to be responsible for day-to-day operations at major seaports and airports for the quarantine clearance of commercial consignments of plants, animals, and agricultural products. The recommendation was accepted by the government, to allow existing high security quarantine stations to continue to be owned and operated by state governments. However, a significant change for plant imports was the recommendation that was accepted by the government to allow private and other commercial interests to own and operate low to medium security quarantine premises. This had a dramatic effect on the way plants were imported into Australia. Up to that stage, most importations of nursery stock to Australia had been made by government employed breeders, with only fewer numbers of plants imported by private nurseries through the government post-entry quarantine stations. Following the change, commercial nursery operators established their own private plant post-entry quarantine nurseries and a great variety of plants with an assessed lower risk profile started to be imported in large numbers. An interesting feature from the review, rejected by the Government of the day, was the concept of full cost recovery. This was based on the broader public good conferred by preventing exotic diseases and pests becoming endemic in Australia that posed a threat not only to agricultural but also to human health (rabies, for example) and the environment.
In 1995, the operational service delivery for plant, animal and human quarantine in Australian States and Territories except Western Australia, Tasmania and the Northern Territory was transferred to the Australian Quarantine and Inspection Service (AQIS). Those latter three jurisdictions continued to deliver national border quarantine services on behalf of and funded by the Commonwealth under formal agreements with AQIS.22
The 1996 Nairn Quarantine Review23 recommended a fresh approach to quarantine with several key themes: managed risk based on science; a continuum of quarantine (pre-border, border, post border); shared responsibility (Government, industry, and the community); consultative decision making; external input to quarantine policy; and enhanced capacity in plant quarantine protection and policy. The review highlighted the imbalance between the animal and plant sectors with respect to quarantine even though the data clearly demonstrated the rate of incursions of plant pests and diseases over the previous twenty-five years was about ten times greater for plant pests compared to animal pests. Following the review, an Australian Plant Health Council and the Office of the Chief Plant Protection Officer position within the department were formed. Since their establishment, the status for plant industries has been enhanced and a greater partnership approach has been fostered between the Commonwealth, States, Territories, and industry. Another major change flowing from the review was adoption of specific recommendations to move from a quarantine border/barrier focus to a broader continuum including pre-border, border, and post-border activities. This emphasised the importance of keeping unwanted diseases and pests offshore as well as placing more attention on the value of surveillance within Australia and on national preparedness for and response to incursions. This ultimately led to the development of the concept of the biosecurity continuum and a culture of shared responsibility between government, industry and the wider community.24 However with sharing of responsibility comes the need to share costs and the report recommended the application of full cost recovery policy for quarantine operations from industry.
In 2008, Australia’s biosecurity system was once again reviewed,25 leading to further transformation. Building on the foundations of the Nairn Report, one of the most significant outcomes from the Beale review was the recommendation and acceptance to establish a new Biosecurity Act. Whilst it took seven years to draft and finalise the legislation, the new Act brought much needed change to a complex regulatory system that had been drafted at the beginning of the twentieth century when travellers and goods only arrived by ship. This new legislation was enacted in 2015, to include ‘protection of the economy, environment and human health from negative impacts associated with entry, establishment or spread of exotic pests and diseases’.
A central tenet of the Beale review was the need to strengthen the partnership approach and reflect the shared responsibility for biosecurity between the Australian Commonwealth, state and territory governments, industry (including importers, exporters, and onshore agriculture, fisheries, and forestry sectors), trading partners and the broader community. Whilst the Australian Government takes primary carriage of pre-border and border operations, each state and territory has legislation and protocols to cover post border biosecurity in their jurisdiction for the detection and management of pests that have breached the national border. In 2012, the Intergovernmental Agreement on Biosecurity was established to strengthen the collaborative approach between the Commonwealth and state and territory governments in addressing Australia’s biosecurity issues. A National Biosecurity Committee was established with its core objective of cooperation, coordination and consistency among the various government agencies involved.26 By their working together, Australia’s national biosecurity system was enhanced and made more sustainable.
Likewise, the government accepted the principle of industry taking a greater role in managing biosecurity risks with support and oversight from the department, thereby reducing the level of intervention and allowing greater flexibility in business operations. The underlying principle was to support those businesses doing the right thing and intervene more with those that did not comply.
From a plant perspective, a major outcome from the Beale review was the recommendation to construct a single national post-entry quarantine facility to consolidate all five existing departmental operated plant and animal post-entry stations into one site. Almost $380 million was allocated over seven years to construct the new Commonwealth-operated post-entry quarantine station based at Mickleham, Victoria, that commenced operations in 2015–6.
Plant pathway risks
All imported planting material and plant products, fresh and dried, presents a risk because they can be infected with or have the capacity to transmit or carry exotic plant pests. The highest plant biosecurity risk is posed by imported live plants as nursery stock for propagation. Invertebrate pests have potential to directly damage plants and to vector significant plant pathogens, particularly plant viruses. Vectors including nematodes, plant sucking insects and mites intercepted at the border, are managed even if already recorded in Australia, due to the potential risk of transmitting exotic pathogens. Imported plants also pose a potential pest in their own right as weeds, with comprehensive assessments conducted as a condition of import for new plant species.
Due to their hardiness and durability, seed and grain have been internationally exchanged across borders for millennia. The plant pathogen risks of seed and grain vary depending on the species, country of import and mode of introduction. The end use is an additional factor as seed and grain imported for sowing and propagation typically present a higher biosecurity risk compared with seed imported for processing and consumption because the product is typically processed or treated in such a manner as to reduce the viability of the seed and/or remove pests that may be present.
The perishable nature of fresh plant products including fresh fruit, vegetables, cut flowers, herbs, and spices intended for consumption typically pose a lower biosecurity risk for disease transmission in comparison to live plants. However, these products may pose a risk of invertebrate pests being present and must be managed. Fresh plant products that carry seeds or are capable of being propagated pose a higher biosecurity risk and generally require additional risk assessment and mitigation.
Dried plant products including dried flowers/foliage, plant-based stockfeed, souvenirs, and ornaments generally pose a lower phytosanitary risk because most plant pathogens require a living host to remain viable. Timber and wooden products including solid wood packaging material (skids, flooring, pallets, and dunnage), logs, woodchips, and manufactured wooden products present a biosecurity risk as they may be infested with a range of significant pests. Decayed and damaged timber is often used in dunnage and solid wood packaging presenting an ideal environment for pest infestation. Excessive bark on timber and wooden packaging further increases the potential risks because many insects and fungal pathogens readily inhabit the microclimate created by the bark. Highly manufactured wooden products, including plywood, veneer or reconstituted wood products such as particleboard and chipboard generally present minimal biosecurity concerns. Nevertheless, viable spores of Austropuccinia psidii (formerly Puccinia psidii), the cause of myrtle rust, were found on plastic-wrapped timber pallets imported to Australia from Brazil in 2004, leading to this pathway being closed to prevent further ingress of the rust into Australia.27 This example highlights the difficulties in managing pathways and emphasises the challenges of enacting a zero-risk biosecurity policy.
Soil deserves special mention because it can readily act as a medium for transporting plant pests including fungal sclerotes, bacterial spores, nematodes in a resting state, and weed seeds of biosecurity importance. Soil can be readily moved in rooted plant material or as contamination on the exterior of cargo containers and transport vehicles including used cars, farm and military machinery, and earth moving equipment. Soil can also be a contaminant on passengers’ personal goods including boots, tents, and bicycles. Live plants imported as bare rooted cuttings must be free of soil to remove the inherent risk associated with this contaminant.
Australia takes a risk-based approach with measures aimed at managing pest risk to an ‘appropriate level of protection’ (ALOP). A ‘no or zero risk’ policy cannot be achieved as it would mean a ‘no trade/tourist’ policy that is indefensible and impossible to achieve given natural pathway risks including migratory birds, trade winds, and ocean currents cannot be managed. Australia accepts a ‘very low level’ of risk as the ALOP necessary to protect our plant health against the harmful effects of exotic pests. Where the risk of pest detection exceeds the ALOP, Australia requires the application of measures to reduce the risk. Measures may include inspections, treatments and other procedures intended to reduce the pest risks. In choosing and applying measures, Australia follows the International Plant Phytosanitary Commission (IPPC) principles of necessity, equivalence and harmonisation. Although prohibition or total ban of trade will reduce the pest risks, this action may encourage people deliberately to bypass quarantine or to smuggle products into the country thus bypassing managed systems and potentially creating a greater risk. Further, prohibition of trade goes against International Sanitary and Phytosanitary (IPPC) efforts to liberalise trade using the least trade restrictive measures. Restriction could result in retaliatory action by trading partners. Consequently, international efforts established the World Trade Organization (WTO) Agreement on the Application of international Sanitary and Phytosanitary Measures to ensure exchange in agriculture and food products is not impeded by trade barriers disguised as phytosanitary measures.28
Plant biosecurity risk pathways
The international transport of commercial and non-commercial cargo and people between countries presents an ongoing and increasing pathway risk for entry of biosecurity pests. Global changes in trade and population migration are causing demands for agricultural products with new plants and plant products being imported from new global trading partners, often with limited biological knowledge of the associated pest risks. For example, international trade in cut flowers into Australia has grown significantly in volume during the last decade and so too has the number of countries exporting these goods. Australia imports approximately 120 million cut flowers and foliage annually. The quantity of imports has increased steadily in the past twenty years and has seen a shift in trade originated from Europe to African and Asian countries becoming the dominant suppliers. The major imported species and exporting countries for cut flowers are roses from Kenya, India, Colombia, and Ecuador; orchids from Singapore and Thailand; chrysanthemums from Malaysia and South Africa; and carnations from China and Vietnam.29 This is presenting new biosecurity risks including pests unknown to science. In 2009, a new genus of thrips was intercepted on cut flowers imported into Australia from Kenya and Ethiopia.30 Interestingly, the thrips species Kenyattathrips katarinae, was named after the biosecurity officer who found the thrips.
Rapid expansion of e-commerce and mail order presents a major biosecurity risk pathway (Table 1). More than 180 million items of international mail are sent to Australia each year with over 400,000 items of biosecurity interest being detected with mail order and Internet purchases making up a significant portion of the seised items.
2019–20 | 2020–21 | ||
---|---|---|---|
Cargo consignments | 58.9 million | 77.2 million | |
Aircraft | 75,830 | 16,206 | |
Vessels | 18,860 | 17,848 | |
Shipping containers | 2.3 million | 2.6 million | |
International travellers | 17.3 millionA | 747,000 | |
International mail items | 94 million | 72.1 million |
In recent years, global changes in temperature and rainfall, combined with increased levels of carbon dioxide, are affecting the distribution of crops and pests thereby impacting biosecurity. Pest lifecycles are forecast to change with the potential for more generations per year (multivoltine) with different seasonal population peaks. This is likely to result in more movement of invertebrates and pathogens, particularly vectors.31 Climate change is predicted to increase the frequency and severity of extreme weather events, and this may increase the likelihood of incursions at national and domestic borders. For instance, increased cyclonic activity in areas where citrus canker, caused by the bacterium Xanthomonas axonopodis pv. citri is present, has expanded the distribution of this important citrus disease in the USA.32
Loss of long-established pest control practices like pesticides and fumigants poses another pathway risk as it will likely lead to increasing presence of pests on plants and plant products exchanged internationally. Deliberate introduction of exotic pests to countries in the form of bioterrorism is another pathway risk that needs to be managed.
Managing plant biosecurity risks
Rapid transport and increased movements of people and goods has magnified the potential for damaging pests to spread globally. These threats are real. Between 2012 and 2017, the annual number of interceptions of biosecurity risk materials at Australian borders rose by almost 50%, to 37,014.33
Australia’s national biosecurity system involves collaborative partnerships across the biosecurity continuum encompassing pre-border, border, and post border programs. The adoption of science-based risk analysis, operational activities, surveillance, and response systems all play an important role in mitigating biosecurity risks from entering, establishing, and spreading in the country.
Pre-border programs
Prevention is better than cure! By managing biosecurity pest risks offshore, the entry risk at the border and post border is reduced. There are a number of ways to achieve this outcome.
Pest risk analysis (PRA) is an essential tool in the biosecurity toolbox and one of the key pre-border programs. PRAs consider the biological, economic and environmental risks associated with pests that may be present on imported goods and develop risk mitigation protocols to reduce the risk of entry. If the pest has a high likelihood of entering, establishing and spreading in Australia and the economic and/or environmental impacts are above the ALOP, then additional risk mitigation systems are required prior to the entry of the goods.
Australia recognises pest-free areas and areas of low pest prevalence where a specific pest does not occur as demonstrated by scientific evidence and/or measures to maintain freedom.34 This allows specific plant products to be exported with a lower level of biosecurity intervention because goods can be certified free of specific regulatory pests and cleared more efficiently. Australia accepts offshore pre-clearance programs with some national plant protection organisations performing pest inspections, testing and treatments in the exporting country. Not only does this reduce the chances of pests entering at the border, but pre-clearance arrangements typically reduce the need for time-consuming and expensive on-arrival border activities, thereby making the process of getting products into Australia more efficient.
Australia works with other national biosecurity agencies to build surveillance and diagnostic capacity amongst our near neighbours and across the globe, to better prevent the risk of pests reaching Australia’s border. International or pre-border surveillance and diagnostic activities aim to provide early warning of new or exotic pests capable of entering Australia and mitigate risks associated with them.
Border programs
Australia’s border security provides a key line of defence against the entry and establishment of exotic plant pests. For more than a century, Australia has managed risks posed by the international trade of plants and plant produce at ‘first ports of entry’ where biosecurity officials clear international aircraft and shipping vessels, including their goods, baggage, crew, and passengers. Regulatory measures used at the Australian border include inspections, treatments, post-entry quarantine, stakeholder engagement and enforcement.
Inspection of regulated goods is the most frequently used procedure employed worldwide to determine compliance with import requirements and detection of pests.35 In Australia, biosecurity officers are located at international and state border entry points including airports, seaports, border road crossings, mail centres, cargo depots, and post-entry quarantine facilities. Inspections can involve reviewing import permits and assessing compliance with regulations to more detailed examinations including diagnostic testing of imported high risk plants. International mail is subject to inspections including visual assessment, X-ray imaging, and trained detector dogs.36 If goods are found to be contaminated with pests, soil or other biosecurity risk material, they are directed for further treatment or other risk mitigation procedures including destruction, re-export, and prosecution may result. Managing the risks of biosecurity items entering on passengers and their baggage at international airports and seaports is complex and difficult. A systems approach is adopted using a range of mitigation processes. Before landing, international aircraft arriving in Australia play an in-flight biosecurity announcement alerting passengers of the importance of declaring prohibited goods. Disembarking passengers are required to complete an incoming passenger card to declare items of biosecurity concern including food, plants, parts of plants, herbs, seeds, wooden articles, and presence of soil attached to tents and shoes. Passengers must also declare whether they have visited high-risk areas such as farms where they may have picked up biosecurity risk items. In this way, a risk assessment of items being carried by passengers can be made by biosecurity inspectors and directed for further assessment or treatment. Passengers must then pass through border controls where detector dogs and X-ray machines are used to screen baggage. The department uses data profiling to target certain events or individuals that may present a potential higher risk pathway: for instance, overseas students returning with risk goods at the start of university terms, those attending special religious events or importers who have a history of non-compliance of importing biosecurity risk items.
Biosecurity inspectors examine goods and verify documents to ensure they meet regulatory requirements. Inspectors may visually assess the goods or use microscopic devices to detect microorganisms and small invertebrate pests and their life stages such as mites and insect eggs. If the goods or paperwork don’t meet import requirements, further risk-mitigation processes may be required depending on the nature of non-compliance. If regulated pests are detected, the inspector may seek specialist advice from entomologists and plant pathologists or direct the consignment for treatment and other biosecurity risk-mitigation measures consistent with import requirements.
Detector dogs are trained to search international mail, passenger’s baggage and imported cargo to detect undeclared biosecurity risk material. Detector dogs are particularly effective in sniffing out live plants, plant produce, and soil. With their enhanced sense of smell and friendly nature, detector dogs proved popular with the travelling public and are now commonly seen at Australian and interstate entry points and used in media campaigns to educate the public on the importance of biosecurity. In 2022, the department celebrated its thirtieth year of the biosecurity detector dog program. On average, biosecurity detector dogs find up to 9000 biosecurity risk items during their eight-year working life. The three most common items the detector dogs find are meat, seeds, and fruit.37
Certain imported plants and plant produce require mandatory treatments to manage the biosecurity risks. Treatments can include fumigation, application of pesticides and disinfectants, irradiation, or physical treatments such as heating, cooling and reconditioning whereby biosecurity risk material is removed from the consignment. Selection of the most appropriate treatment depends on the pest species detected, commodity and intended use of the goods.
The international movement of live plants and seed for breeding and crop improvement has significantly contributed to the development of Australia’s prosperous agricultural system. However, trade in live plants pose special biosecurity challenges due to their capacity as living hosts to introduce biosecurity pests that may not be obvious at the entry point particularly for viruses and viroids. Biosecurity risks posed by live plants vary depending on the species susceptibility to exotic pests, economic and ecological impact of the pest on crops and native flora, country of origin, and type of plant material imported. Seed poses a relatively lower risk compared to rooted plants although, an incursion from an imported seed lot can be immediate, widespread, and an enduring economic cost for a commodity. This was evident in the detection of quarantine pathogen Cucumber green mottle mosaic virus (CGMMV) in 2014 in the Northern Territory where emergency measures were introduced to mitigate the risk of any further introductions of CGMMV into Australia.38 CGMMV was subsequently detected including in mail ordered seed consignments,39 however the systems-based risk management approach now applied to cucurbitaceous vegetable seeds demonstrates Australia’s ability to provide an ALOP.40
Import conditions for live plants vary from simple visual screening on arrival to mandatory treatments and extensive pathogen testing in PEQ facilities. Live plants are typically classified into two or more risk categories. Lower risk plants include many ornamental species that are not hosts of significant plant pests. These plants are commonly imported in tissue culture under sterile conditions, and the likelihood of regulated pests is largely mitigated and may simply require visual inspection on arrival. If no obvious pests or diseases are present, they can be released without further biosecurity intervention. If the same ornamental plants are imported as bare rooted cuttings, there is a greater risk of biosecurity pests being present and additional mitigation steps, including treatment and growth in PEQ with disease screening, may be required. Higher risk plants include many commercial fruit and berry crops, amenity and forest tree species and ornamental hosts of significant plant diseases that may damage an industry or the environment. Higher risk plants usually require active testing for the causal agents of these diseases and are typically directed to government PEQ facilities given the higher level of containment and diagnostic expertise required to perform pathogen testing.41 Australia also recognises high health-planting sources as centres of excellence. These centres provide a high level of compliance with Australia’s regulatory requirements and biosecurity interventions on material sourced from these suppliers can be significantly reduced or waived.
Public awareness and engagement by all stakeholders is essential to deliver an effective biosecurity program. The COVID-19 pandemic brought biosecurity and the dangers posed by exotic pests and diseases into sharp focus for many Australians. Without active support by the broader community, biosecurity outcomes can be jeopardised by ignorance and non-compliance. The department has many public awareness campaigns in place noting the TV show Border Security Australia’s Front Line is greatly contributing to people’s awareness of the importance of biosecurity. Likewise Australians travelling interstate are always reminded of the importance of being biosecurity aware as they cross the state borders. A further objective of public awareness campaigns is to educate the community about the complexity and difficulty in managing all risk pathways and the concept of managed risk to the aforementioned ALOP. This message is important otherwise the community may develop unrealistic expectations and become overly critical when an exotic pest bypasses the border.
Human side of plant biosecurity
In 2014, two Australian journalists found themselves in the middle of the crash site of Malaysian Airlines plane MH17 in Ukraine.42 They decided to collect seeds from the local sunflower plants growing at the crash site and distribute them to the families and friends of the thirty-eight crash victims from Australia. However, what they saw as a humane gesture, Australian biosecurity staff saw as a challenge to Australia’s strict biosecurity protection regime. Contacts were made with the journalists and seeds procured from the field site made their way to the department’s Plant Quarantine nursery at Knoxfield. On arrival, the sunflower seeds were found to be of low quality with many seeds dry, poorly developed, and shrivelled. The Knoxfield team first tried germinating the seeds on cotton wool, without success. Next, a batch of seed was hot water treated. Of the 1000–2000 seeds treated, only 40–50 germinated. The best of these seedlings were potted separately in secure, quarantine glasshouses and after a few months, the plants matured and were found free of exotic diseases to Australia. Seeds were harvested from these plants, and returned to the journalists who distributed the seeds to the families and friends of the MH17 disaster. A seemingly small act but touching for all involved.
Individuals are responsible for being aware of and complying with Australia’s biosecurity regulations. The department has an active compliance branch that contributes to the integrity of border operations through investigation and enforcement activities. Likewise, State and Territory governments have biosecurity statutory powers whereby regulatory officers have the authority to impose fines for individuals who contravene biosecurity regulations.
Timely and accurate pest identification and risk mitigation advice is crucial to the delivery of effective border operations.43 In line with international agreements, regulatory action can only be justified if the pest is of biosecurity significance. Some interceptions are unexpected and are new to science.44 Access to plant diagnostic specialists including entomologists, plant pathologists and botanists is a key element in identifying pests, pathogens and weeds and in providing timely and science-based decisions.
Post-border programs
While Australia boasts a strong biosecurity system, given the rapid movement of plants, goods and people around the globe, the risks of biosecurity pests approaching and breaching Australia’s borders are ever-present. Post-border programs, including surveillance and monitoring of new pest incursions and rapid response programs, play an integral role in the biosecurity continuum minimising the impact of pests through early detection, eradication and containment.
Being surrounded by an ocean, the internal domestic movement of people and goods across borders is easier to regulate compared with countries that share international land borders where controlled movement of people and plant products across borders is more difficult. Each State and Territory government has legislation in place to help mitigate the spread of plant pests across borders.
In Australia, all levels of government along with industry and the community conduct post-border surveillance programs to detect new incursions, delineate spread of new outbreaks, and to gather ‘evidence of absence’ data to show overseas trading partners Australia’s maintenance of pest area freedoms. Surveillance programs include sentinel site surveys, structured and passive surveys and programs to educate the broader community such as fruit fly programs and free of charge service for pest identifications.
Should an incursion of an exotic plant pest occur, Australia has well-established response arrangements in place. Working in close partnership with State, Territory and industry stakeholders, the department coordinates the Australian government’s actions in responding to the detection of, and implementation of emergency responses to, incursions of exotic pests. Following the 1996 Nairn review, plant industry organisations, along with all levels of government established Plant Health Australia (PHA) to take a partnership approach to plant health issues and enhance Australia’s national ability to deal with plant pest incidents.45 In 2005, PHA established the world’s first Emergency Plant Pest Response Deed (EPPRD) that increased Australia’s capacity to respond to emergency plant pest incursions in a timely, effective and efficient manner including potentially funding reimbursement costs for growers.46 The deed is underpinned by PLANTPLAN, a national emergency preparedness and response plan for plant industries. It formalises the role of plant industries’ participation in decision making, as well as their contribution towards the costs related to emergency responses.
Following an incursion event, a Consultative Committee on Emergency Plant Pests (CCEPP) is formed between the Commonwealth, states and territories, industry, Plant Health Australia and the National Management Group for plant pest emergencies meets. This group works with a Scientific Advisory Panel to evaluate the technical feasibility and cost efficiency to determine if eradication of a recently entered pest is possible.
Industry-led surveillance programs play an important proactive approach to early detection and response plans. Likewise industry-wide biosecurity plans and on-farm biosecurity awareness are key post border biosecurity tools. Identifying pests that pose the highest risk and their potential to enter, establish, and spread within Australia enables efforts and resources to target the highest risks and implement mitigation and preparedness activities. In 2019, Australia’s national Plant Health Committee, a sub-committee of the National Biosecurity Committee (NBC), agreed to focus national preparedness capability on the top forty-two national priority plant pests (NPPP). The subsequent development and implementation of nationally agreed priority plant pest action plans, such as plan to prevent the introduction of the bacterium Xylella fastidiosa and its exotic vectors, is overseen by these committees and are a national resource demonstrating Australia’s implementation of the Intergovernmental Agreement on Biosecurity (IGAB) and the National Plant Biosecurity Strategy (NPBS).47
Looking to the future
Despite a highly robust and formidable biosecurity system, Australia is facing growing biosecurity risks that are becoming more complex and harder to manage. Exotic pests and diseases are spreading around the world and putting unprecedented pressure on Australia’s borders. Goods and passengers coming into Australia are predicted to double over the next decade48 placing increased pressure on the biosecurity system. The department can no longer rely on linear, transactional processes as biosecurity risk pathways become increasingly complex and multifaceted.
The department is therefore reforming the biosecurity system to strengthen Australia’s ability to keep out biosecurity pests while minimising regulatory burden and enabling goods to be moved across the border quickly and efficiently. In 2021, the department released Commonwealth Biosecurity 2030, providing a clear roadmap to guide the department’s efforts towards building a stronger, smarter and more sustainable biosecurity system.49 Commonwealth Biosecurity 2030 outlines how the department will build our capability to address these threats, including strengthening partnerships with stakeholders. Continued refinement of the risk-based biosecurity system enables the department to build on existing practices whilst modernising processes to effectively, efficiently, and sustainably protect Australia from exotic pests and diseases. Nine strategic actions were identified to support the 2030 goals and adapt Australia’s biosecurity system for the future.50 The success of our biosecurity system relies on all parties working collaboratively and partnering with industry and other stakeholders to design, pilot, and implement continuous improvements. This will be critical to achieving reform and assuring continued confidence in the management of biosecurity risks.
A crucial component of Australia’s national biosecurity system is an efficient and effective diagnostics system to rapidly identify harmful pests and diseases at the border and effectively manage these risks. In the same year the Commonwealth Biosecurity 2030 roadmap was released, the government funded a four-year, $22 million program to update and modernise the department’s plant diagnostics capacity and capability.51 This program has enabled innovative improvements to all aspects of the department’s diagnostic capability, supporting post entry plant quarantine as well as testing goods through inspection and surveillance activities nationally.
Recent activities delivered under the program include adoption of MALDI Biotyper Sirius technology at the DAFF laboratory in Sydney52. This instrument is now used routinely for preliminary identification of bacteria and fungi in plant samples intercepted at the border, improving the efficiency and timeliness of the department’s border diagnostics.53
In 2017, the department established the Plant Innovation Centre (PIC), an in-house research and development (R&D) capability at the national PEQ facility in Mickleham. PIC offers the department ready access to laboratory facilities to address a range of plant biosecurity challenges. The operationally focused, biosecurity R&D activities are delivered in-house and in collaboration with external providers (research agencies, universities and the business sector). One such project was the adoption of High Throughput Sequencing (HTS) for plant diagnostics in PEQ. The HTS work was a collaborative effort with the diagnosticians across the departments Science and Surveillance Group laboratories, and external parties from Queensland University of Technology, Agriculture Victoria, Hort Innovation, and the New Zealand Ministry of Primary Industries. Almost a decade was spent optimising the HTS methodology, comparing and validating the test against existing diagnostic platforms and developing regulatory policies. From December 2022, the department started implementing the molecular sequencing tool that can identify all plant viruses and viroids from a single sample with unprecedented efficiency.54 This is replacing conventional testing methods like polymerase chain reaction and biological indexing to detect pathogens in plants imported into Australia.
PIC has developed close collaborative links with the education sector to enhance the departments’ visibility as an employer of choice for high-performing graduates. The department now has formal agreements in place with five Australian universities, co-supervising PhD and masters projects at PIC, furthering the development and modernisation of plant diagnostic capability. In future years, the ongoing commitment to student engagement is intended to better align direction and strengthen our partnerships with Australian universities for sustained capability development.
Changing diagnostic technology
A historical reason for using PEQ to screen imported plants is to allow plants to undergo a period of active growth over extended periods of time (months to years), thereby allowing disease symptoms to develop if pathogens are present. Plant pathologists regularly inspect every plant growing in PEQ for disease symptoms and this justifies the removal of diseased plants. Visual inspection is relatively easy when symptoms are characteristic of a specific disease, but many factors such as pathogen strain, host plant cultivar or variety, time of infection, and the environment can influence the symptoms exhibited. Plants can also exhibit disease-like symptoms as a response to unfavourable abiotic factors such as nutritional imbalances, pest damage, air pollution, or pesticide injury. Other pathogens, particularly viruses, can produce no apparent symptoms and this justifies the emphasis of PEQ diagnostics on viruses. It is therefore necessary to perform additional confirmatory tests in PEQ to aid the detection of exotic pathogens.
A comprehensive range of traditional and modern diagnostic approaches have historically been employed in plant post entry quarantine facilities using bioassays, serological, and molecular techniques.55 Whilst these techniques have been effective, they are time consuming, resource intensive and expensive. Bioassays in particular present challenges in interpreting the symptoms and are being replaced with more timely, accurate, and reliable methods. Polymerase chain reaction (PCR) testing plays an important role in PEQ diagnostics, and although modest efficiency dividends have been realised with the arrival of quantitative PCR and automation, limitations exist with their implementation. There is a lack of internationally accepted and validated molecular diagnostic tests available for biosecurity priority pests, and automation is limited in its scalability due to the large variety of commodities that undergo PEQ and the ever-evolving lists of pests to be tested for. In addition, PCR assays rely on prior knowledge of the plant pest’s genetic makeup to develop new tests, which is why molecular tests have traditionally been complemented with bioassays that provide a more generic approach for assessing presence of plant virus symptoms. The application of diagnostic tools in PEQ for testing viruses and viroids with increased limits of detection and specificity, including HTS, increases confidence in negative data, and in some cases has prompted prompting reduced PEQ periods for specific plant imports.
An example of the changing world of delivering PEQ diagnostics is seen using the fastidious bacterial genus Xylella, number one on Australia’s High Priority Plant Pest List, as a case study. Prior to mid-1990s detection of Xylella was through direct visual observation of plant disease symptoms over long periods of time in PEQ along with use of bioassays sensitive to infection. Hot water treatment (HWT) was also used to eliminate the causal agent. In the late 1990s, a commercial Enzyme-Linked Immunosorbent Assay (ELISA) was used to screen imported plant hosts for Xylella fastidiosa. In the early 2000s, a PCR test was introduced into PEQ for high-risk imported genera. In 2015, giving the expanding host range and spread of the disease overseas, the department introduced a range of emergency measures to target known plant host families with two PCR tests or HWT required.
Conclusion
Whilst the advent of modern transport systems and greater global trade in live plants and plant products has brought significant benefits for trading nations, it has increased the global movement of pests including invertebrates, pathogens and weeds. Australia’s plant biosecurity system has undergone many changes and will continue to evolve and mature. There are many plant biosecurity risk pathways, and no plant biosecurity program can be completely zero-risk. Minimisation of these threats through an effective biosecurity system is essential to support and protect Australia’s agricultural producers and unique flora. Modern risk mitigation combining pre-border, border and post-border programs across the biosecurity continuum are essential. Post-entry plant quarantine combined with modern diagnostics plays a key role in enabling the safe and timely access of new plant genetics to ensure our industries remain competitive, profitable and sustainable. To be successful, biosecurity needs to be adopted and practiced by all stakeholders.
Acknowledgements
The authors acknowledge and thank Dr Andrew Geering for helping to review the manuscript and providing links to the history of quarantine.
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Footnotes
† This paper belongs to the Special Issue ‘History of Plant Pathology in Australasia’ (Historical Records of Australian Science Volume 35 Number 2), but was not published in time for inclusion in the online special issue.
4 Mack (2003).
10 Anonymous (1804).
11 Anonymous (1861).
14 Anonymous (1866, 1869a).
16 Anonymous (1867).
17 Anonymous (1878).
18 Anonymous (1886).
19 Anonymous (1895).
20 Anonymous (1898).
21 Anonymous (1908a, 1908b).
22 Anonymous (2002).
30 Mound (2009).
31 Jones (2009).
33 Anonymous (2018).
34 ISPM 4 (1996).
35 ISPM 23 (2005).
40 Anonymous (2020).
45 Donovan (2004).
54 Anonymous (2022).