Journal of Botanic Gardens Conservation International

Volume 17 • Number 1 • January 2020

Celebrating International Year of Health: Botanic gardens and biosecurity Volume 17 • Number 1

IN THIS ISSUE... EDITORS

EDITORIAL: BOTANIC GARDENS AND BIOSECURITY .... 03

FEATURES

Suzanne Sharrock Kate Marfleet Director of Global Seed Conservation and Plant Programmes Health Network Coordinator NEWS FROM BGCI .... 05

PLANT HUNTING TALES: RECORDING INVASIVE ALIEN PLANT Cover Photo: Colorado Potato Beetle (Leptinotarsa decemlineata) (Pixabay) PESTS IN MONTSERRAT, WEST INDIES .... 08

Design: Seascape www.seascapedesign.co.uk FEATURED GARDEN: BOTANICAL GARDEN “JEVREMOVAC”, BELGRADE, SERBIA .... 11 BGjournal is published by Botanic Gardens Conservation International (BGCI). It is published twice a year. TALKING : INTERVIEW WITH PROFESSOR NICOLA SPENCE, Membership is open to all interested individuals, institutions DEPARTMENT FOR ENVIRONMENT, FOOD AND RURAL AFFAIRS, UK 14 and organisations that support the aims of BGCI. ....

Further details available from:

• Botanic Gardens Conservation International, Descanso House, 199 Kew Road, Richmond, Surrey TW9 3BW UK. Tel: +44 (0)20 8332 5953, Fax: +44 (0)20 8332 5956, E-mail: [email protected], www.bgci.org

• BGCI (US) Inc, The Huntington Library, Art Collections and Botanical Gardens, 1151 Oxford Rd, San Marino, CA 91108, USA. Tel: +1 626-405-2100, E-mail: [email protected] ARTICLES Internet: www.bgci.org/usa

• BGCI (China), C/O South China Botanical Garden, CAS 723 Xingke Rd. Guangzhou, 510650, Guangdong, China THE INTERNATIONAL PLANT SENTINEL NETWORK Tel: (86)13662496295, Email: [email protected] Kate Marfleet and Suzanne Sharrock .... 17 www.bgci.org/china/

• BGCI (Southeast Asia), Jean Linsky, BGCI Southeast Asia Botanic Gardens Network Coordinator, WHAT ROLE CAN BOTANIC GARDENS AND ARBORETA PLAY IN Dr. Cecilia Koo Botanic Conservation Center, UNDERSTANDING THE RISK THAT HARMFUL ORGANISMS POSE No. 31, Tongsing Rd., Gaoshu Township, Pingtung County TO PLANT HEALTH? Charles Lane and Laura Stevens .... 21 90646, Taiwan, China. Tel: +886 8 796 0913, Mobile: +886 966484475, Email: [email protected], Internet: www.bgci.org; www.kbcc.org.tw/en THE BELGIAN PLANT SENTINEL NETWORK Anne Ronse 24 .... • BGCI (Africa), Kirsty Shaw, BGCI Africa Office, IUCN Eastern and Southern Africa Regional Office (ESARO), THE GROWING ROLE OF BOTANIC GARDENS IN MITIGATING P.O. Box 68200 - 00200, Nairobi, Kenya, Tel. +254 David AJ Teulon (0)725295632 Skype: bgci_kirsty, Email: THE IMPACT OF INVASIVE ALIEN .... 27 [email protected], Internet: www.bgci.org

• BGCI (Russia), c/o Main Botanical Gardens, RISKS OF PEST AND DISEASE MOVEMENT VIA PLANT AND Botanicheskaya st., 4, Moscow 127276, Russia. SEED EXCHANGES Tel: +7 (095) 219 6160 / 5377, Fax: +7 (095) 218 0525, Iva Franić, Eric Allan, Simone Prospero and René Eschen 30 E-mail: [email protected], www.bgci.ru ....

BGCI is a worldwide membership organisation established in 1987. Its mission is to mobilise botanic gardens and ROSE ROSETTE VIRUS AND ITS POTENTIAL RISK engage partners in securing plant diversity for the well- Ines-Vazquez-Iglesias, Gerard Clover, Rebekah Robinson, being of people and the planet. BGCI is an independent Adrian Fox, Neil Boonham .... 33 organisation registered in the United Kingdom as a charity (Charity Reg No 1098834) and a company limited by guarantee, No 4673175. BGCI is a tax-exempt 501(c)(3) TRAP PLANTS AS PLANT SENTINELS Uwe Starfinger .... 37 non-profit organisation in the USA and is a registered non- profit organisation in Russia. BIOSECURITY BEYOND QUARANTINE: THEMES FROM Opinions expressed in this publication do not necessarily THE 2020 PLANT HEALTH ISSUE OF SIBBALDIA reflect the views of the Boards or staff of BGCI or of its members. Katherine Hayden .... 40

BGCI • 2020 • BGjournal • Vol 17 (1) 02 EDITORIAL: PLANT HEALTH

Dear BGjournal While this work was carried out with Reader, support from project funding, the Belgian case study also proposes a long term As 2020 is the solution to mainstreaming plant sentinel International Year detection through co-ordination of of Plant Health, it is activities through the Belgian Association appropriate that the of Botanic Gardens and Arboreta. theme of this issue of BGjournal is From Belgium we cross half the world to biosecurity and plant pests and diseases. New Zealand (p. 27), a country where Red palm weevil found in China (IPSN) This is a particularly important topic as the biosecurity is taken so seriously that the combination of a changing climate and Government’s advertising campaign Further examples of biosecurity measures greater movement of plant material across suggests that all 4.7 million citizens of botanic gardens can take are provided in borders has exacerbated such problems New Zealand should be preventing the the article by Katherine Hayden (p. 40). in recent years. Our particular focus is on arrival and spread of pests and diseases. the role of botanic gardens in detecting, Here, another important role of botanic Our plant hunting tale this edition is not preventing and managing threats from gardens is highlighted – that of raising a plant hunting tale at all. Instead, it is new pests and diseases. public awareness of the risks associated about finding bugs on plants - Invasive with pests and pathogens, and Alien Species to be precise, and in Our first article (p. 17) describes the educating people about not inadvertently Montserrat in the West Indies (p. 8). International Plant Sentinel Network (IPSN), introducing them to New Zealand. Finally, the BGjournal interview is with which is co-ordinated and managed by Auckland Botanical Garden’s Biosecurity Professor Nicola Spence, Chief Plant BGCI. The IPSN comprises more than 50 Trail is an excellent example of this. Health Officer at the Department for botanic gardens and arboreta who provide Environment, Food and Rural Affairs, UK an early warning system for emerging Another approach to early detection who tells us all about the International pests and diseases by screening non- that lends itself particularly to botanic Year of Plant Health (IYPH). IYPH in 2020 native plants in their collections for pests gardens is the use of trap plants as is a once in a lifetime opportunity to raise and diseases that are prevalent in their sentinels. These are plants that are global awareness on how protecting plant region, and alerting partners in the native particularly attractive to pests and health can help end hunger, reduce ranges of those species if susceptibility is pathogens. This is the focus of the poverty, protect the environment, and detected. In our second article (p. 21) article by Uwe Starfinger (p. 37), who boost economic development. Events are Charles Lane and Laura Stevens explain points out that botanic gardens with being organised around the world to how the IPSN is being used by the UK their wide range of collections are celebrate IYPH and to highlight the vital plant health authorities to carry out particularly suited to carrying out this role of national and regional plant health research on a range of pests included on type of work. organisations in protecting plants from the UK’s pest risk register. damaging pests and diseases. Clearly, As well as being an important part of the we have an important role to play in Our third article (p. 24) is an example from solution, botanic gardens can be part of botanic gardens, and we need to play our Belgium, where the team carried out the problem. In their article on the risks part in this initiative. systematic on-site sampling in the of pest and disease movement via plant collections of participating gardens for and seed exchanges (p.30), Iva Franić I hope you enjoy this edition of BGjournal several suspected pests and pathogens. and co-authors make a series of and, as ever, we welcome your feedback As a result, two of the targeted organisms recommendations about how botanic and ideas. were recorded for the first time in Belgium: gardens might exchange seeds and the phytoplasma ‘Candidatus Phytoplasma plant material more safely to minimise Paul Smith ulmi’ and the fungus Sirococcus tsugae. these risks. Secretary General BGCI

BGCI • 2020 • BGjournal • Vol 17 (1) • 03 03

FEATURES NEWS FROM BGCI

BUG HUNTING TALES: RECORDING INVASIVE ALIEN PLANT PESTS IN MONTSERRAT, WEST INDIES

FEATURED GARDEN: BOTANICAL GARDEN “JEVREMOVAC”, BELGRADE, SERBIA

TALKING PLANTS: INTERVIEW WITH PROFESSOR NICOLA SPENCE

Olive tree affected by Xylella fastidiosa (Jekatarinka/Shutterstock)

BGCI • 2020 • BGjournal • Vol 17 (1) 04 FEATURE

NEWS FROM BGCI

Here we present a selection of the most recent news stories from BGCI. Please browse our website to keep up-to-date with the latest news and events from BGCI and the botanic garden community. www.bgci.org

The meeting was organized within the Each accreditation program, however, Global Botanic Garden Fund context of international stakeholder supports different target audiences. BGCI consultations on the post-2020 global Botanic Garden Accreditation recognises Launched in 2019, BGCI’s Global Botanic biodiversity framework, to discuss and botanical institutions with a focus on Garden Fund (GBGF) aims to support review the future of the Global Strategy plant conservation and sustainability, plant conservation activities, especially for Plant Conservation (GSPC). while ArbNet Arboretum Accreditation in smaller gardens. The Fund also Participants expressed strong support is tailored to gardens with a strong focus administers restricted grant funding for the continuation of the GSPC beyond on woody plants and trees. through the BGCI/ArbNet Partnership 2020 and for this to be increasingly Programme and the BGCI/Minnesota mainstreamed into national and Under this new reciprocal agreement, Landscape Arboretum Grants. international biodiversity frameworks. those applying for BGCI’s Botanic Garden Accreditation who wish to In the first year of the fund, BGCI BGCI is working with the Global be considered for ArbNet Arboretum received 72 applications from 64 Partnership for Plant Conservation to Accreditation will be required to answer institutions located in 39 countries. develop new and updated targets for additional questions related to their focus As a result, 17 grants totalling $33,013 the GSPC, in line with the Convention on woody plant and tree species. have been awarded. Of these, eight of Biological Diversity’s (CBD) proposed grants were provided through the post-2020 biodiversity targets. Those applying for ArbNet Arboretum unrestricted funding of the GBGF, four Accreditation at Level III or IV who wish through the BGCI/Minnesota Landscape BGCI and ArbNet announce to be considered for BGCI’s Botanic Arboretum Grants and five through the reciprocal accreditation Garden Accreditation will be required to BGCI/ArbNet Partnership Programme. answer additional questions on their plant Both BGCI and ArbNet offer accreditation conservation and sustainability activities. The full list of successful applications schemes that recognise standards for can be seen on the BGCI website: leadership, collections management, Gardens that have achieved BGCI https://www.bgci.org/news-events/2019- horticulture, public education, research, accreditation since the last issue of global-botanic-garden-fund-grant-winner staff, and networking. BGjournal: s-announced/

World Forum on the Global BGCI Accredited Botanic Garden Strategy for Plant Conservation Eden Project Institute of Botany, Czech Academy of Sciences From October 28-29, 2019, the China Botanical Garden of Vilnius University Wild Plant Conservation Association Rotterdam Zoo and Botanical Garden (CWPCA) together with the Biodiversity Cambridge University Botanic Garden Committee, Chinese Academy of Jardin Botanique de Montréal Sciences, BGCI, the Global Partnership Botanical Garden of Klaipeda University for Plant Conservation (GPPC), Auckland Botanic Gardens International Union for Conservation of National Tropical Botanical Garden Nature (IUCN), and SEE Foundation Giardino Botanico di Oropa organized the 2019 World Forum on the BGCI Accredited Advanced Conservation Practitioner Global Strategy for Plant Conservation, in Dujiangyan City, China. More than Conservatoire et Jardin Botaniques de la Ville de Genève 260 participants from all over the world The Morton Arboretum attended this meeting.

BGCI • 2020 • BGjournal • Vol 17 (1) • 05-07 05 well-known favourite, Ginkgo biloba) Ana Sandoval for International Plant and all 158 Dipterocarp species endemic Conservation and Benjamin Ong for to Borneo. Analysis of the Bornean Education in Botanic Gardens. The species shows that 60% are threatened awards were presented at an event in in the wild, with 16 species assessed as London on October 8th. Critically Endangered, 34 as Endangered and 46 as Vulnerable. The major threats to these trees are logging and conversion of land to transport corridors and agricultural space e.g. palm oil plantation.

Further information is available at: https://www.bgci.org/news- events/bumper-year-for-tree-assessments -on-the-iucn-red-list/

Global Tree Specialist Group honoured by IUCN Bumper year for tree Ana Sandoval receiving the Marsh Christian award for assessments BGCI has hosted the secretariat for the International Plant Conservation Global Tree Specialist Group (GTSG) Over a third of tree species now have a for over 10 years and at the 2019 IUCN Ana Sandoval works as a technical global extinction risk assessment available Species Survival Commission (SSC) researcher at the seedbank of the on the IUCN Red List of Threatened Leaders’ Meeting, members of the Global Instituto de Investigaciones Species. In the latest IUCN Red List Tree Specialist Group were recipients of Agropecuarias (INIA) in Vicuña, Chile. update (2019.3) over 3,000 assessment several IUCN SSC awards. These awards While the seedbank focuses on the for trees were published, bringing the total are given to recognize the exemplary conservation of crop wild relatives, Ana’s number of tree assessments available on voluntary contribution of individuals and interests and knowledge have enabled the IUCN Red List to 20,116. This is 34% Specialist Groups towards the global her to utilise the facilities of the seedbank of global tree diversity. This means that in work of IUCN. to the maximum, using it to also conserve 2019 over 8,000 assessments for trees seeds of three highly threatened Chilean have been published towards the Global The Harry Messel endemic tree species. Tree Assessment (GTA). Award for Conservation Highlights in the latest update include Leadership was assessments for all Eucalyptus species, received by Malin of which 25% are threatened with Rivers, Head of extinction. With 826 species, Eucalyptus Conservation is the third largest tree in the Prioritisation at world; these assessments therefore BGCI. Malin is provide a major contribution to our global also secretary of GTSG and the award knowledge of trees. recognises her key role in coordinating the Global Tree Assessment (GTA) and Other highlights include the completion of her innovative management of the Benjamin Ong guiding primary school children at the assessments for all twelve monotypic tree initiative. The GTSG were the recipients screwpine (Pandanus) clump at the fringes of Rimba families (of which six are considered of The SSC Chair’s Citation of Ilmu’s central wetland threatened with extinction, including the Excellence, in recognition of the ‘outstanding contribution the GTSG has In Malaysia, Benjamin Ong founded and made in delivering the Species Strategic developed the Rimba Project, a platform Plan between 2017 and 2018’. During this for community engagement and volunteer period, over 2,000 assessments for trees development. He helped Rimba Ilmu were added to the IUCN Red List. overcome resource constraints by training student volunteers as junior BGCI announces 2019 Marsh nature guides, building skills in award winners communication and teamwork, while tripling Rimba Ilmu’s capacity to The Marsh Awards are awarded annually accommodate guided tours. He also by the Marsh Christian Trust, in facilitated novel approaches in garden partnership with BGCI, in recognition of interpretation, including two volunteer-led excellence in International Plant programmes, the creation of two new Conservation and Botanic Garden interpretive trails and Rimba Ilmu’s first Rubiaceae Calycophyllum in Rio botanic garden Education. In 2019, the winners were garden theatre performance.

BGCI • 2020 • BGjournal • Vol 17 (1) 06 New resources to support plant health

The International Plant Sentinel Network (IPSN) has released three new resources to increase awareness and aid identification of a number of priority plant pests/pathogens. These include: three wood boring beetles (Polyphagous Shot Hole Borer, Gold Spotted Oak Borer and Two Lined Chestnut Borer) on European Quercus species, Emerald Ash Borer and Ash Dieback on non-Fraxinus hosts and Rose Rosette Virus. It is hoped that these resources will help botanic garden staff and the general public to identify these damaging pests/pathogens. The Participants of the first South American Botanic Gardens Network Workshop (Noelia Alvarez) resources have been developed in collaboration with UK plant health experts First South American Botanic BGCI’s and each includes information on the Gardens Network Workshop: PlantSnap background of the pests/pathogens in Initiative question, host species, symptom ID and In December, BGCI in collaboration with who to contact if you observe symptoms. the Universidad del Tolima and the BGCI has partnered Botanic Garden Alexander von Humboldt with PlantSnap on The resources can be found at organized a meeting to bring together the creation of https://www.plantsentinel.org/news/1547/. the South American botanic garden possibly the most community and promote the creation comprehensive New education resources of a new botanic garden network in the database of plant region. The event was attended by more photos and As part of the LearnToEngage project, than 40 participants from countries such geolocational data in BGCI and partners have developed four as Argentina, Brazil, Chile, Colombia, the world. PlantSnap 12-week blended learning modules and Guyana, México, Paraguay, Perú, is the most have made the resources for these Suriname, Uruguay and Venezuela. Talks technologically advanced, comprehensive modules available, open access. were presented by all the attendees on and accurate plant identification app ever Each module consists of a trainer and achievements, challenges and created. It gives you a whole new way to participant handbook and also includes opportunities at their botanic gardens. explore the natural world in your everyday online resources which are hosted on The need for the creation of a South life. BGCI has partnered with PlantSnap RBGE’s PropaGate Learning platform. American Botanic Garden Network was so that our member gardens can offer the The four modules are Interpretation, agreed by participants, and an action app to their visitors. Let’s empower Working with diverse audiences, plan to be implemented by the attendees garden visitors worldwide to become Science communication and Evaluation was drafted. citizen scientists in their own communities. and research.

The module resources can be accessed at: https://www.bgci.org/resources/bgci- How do you get involved? tools-and-resources/learntoengage-modu le-resources/ 1. Let us know you’re interested by sending an email to [email protected]. 2. Update your plant list in PlantSearch. 3. We’ll send an agreement for you to sign. 4. We’ll do a video call with key people from your team, helping you get a plan together to introduce PlantSnap at your garden. 5. We’ll send a set of marketing materials you can easily customise including a download link connected to the initiative. 6. We’ll help you launch the app at your garden. 7. Every month you’ll receive demographic data of all visitors to your garden who download the app, along with all plant images (fully verified and identified) taken by your visitors. 8. You’ll get ongoing marketing tips to help ensure the success of the app at your garden.

LearnToEngage modules

BGCI • 2020 • BGjournal • Vol 17 (1) 07 FEATURE Author: Chris Malumphy

BUG HUNTING TALES RECORDING INVASIVE ALIEN PLANT PESTS IN MONTSERRAT, WEST INDIES

Soufrière Hills, Montserrat, West Indies

Montserrat active and an exclusion zone has been Impact of Invasive Alien Species imposed over the southern half of the to the Caribbean UKOTs ontserrat is one of five UK island because of the size of the existing Overseas Territories (UKOTs) in volcanic dome and the risk of pyroclastic Invasive alien species are a major cause of Mthe Caribbean. The others are activity. Montserrat has many unspoiled biodiversity loss globally and their impacts Anguilla, British Virgin Islands, Cayman natural landscapes, due in part to a small are often most severe on island ecosystems. Islands and the Turks and Caicos human population (about 5,000), low Island species or populations are often more Islands. These are former British colonies number of tourists, little development vulnerable because of their previous that have retained their British citizenship compared with most other Caribbean isolation from predators, diseases or and remain part of the United Kingdom. islands, rugged mountainous terrain, competitors. There have been some recent Montserrat forms part of a chain of and restricted access to half the island. catastrophic declines of native plants in the islands known as the Lesser Antilles Consequently, it supports a diverse Caribbean UKOTs which are directly in the eastern Caribbean Sea on the range of unique ecosystems and habitats attributable to the introduction of invasive boundary with the Atlantic Ocean. It is a that sustain many rare and threatened species. For example, the introduction of relatively small island, 16 km long and 11 plant and species. The pine tortoise scale (Toumeyella parvicornis) km wide, and consists of a mountainous invertebrate fauna is particularly rich, has resulted in the 90-95% decline of the interior surrounded by a flatter littoral and it is estimated that 120 invertebrate dominant tree species, Caicos pine (Pinus region. It is nicknamed "The Emerald species are endemic to Montserrat. caribaea var. bahamensis), in parts of the Isle of the Caribbean" both for its Many of these are highly vulnerable to Turks and Caicos Islands. The Caicos pine resemblance to coastal Ireland and the introduction of invasive alien species is the foundation species of the pine yard for the Irish ancestry of many of its which have the potential to negatively habitat, a globally endangered ecosystem inhabitants. In 1995, the previously impact biodiversity, the economy and on which many other plants, birds, reptiles, dormant Soufrière Hills volcano became human health on the island. and depend.

BGCI • 2020 • BGjournal • Vol 17 (1) • 08-10 08 recorded for the first time from Montserrat. One of the most significant pests detected was the Asian citrus psyllid (Diaphorina citri), which vectors the motile bacterium, Candidatus Liberibacter spp., causing Citrus greening or Huánglóngbìng. This is one of the most important pests of citrus worldwide. The disease was first detected in Florida in 2005 and within three years, it had spread to the majority of citrus farms, and devastated commercial citrus The remains of a Pinus caribaea forest in the Turks and Caicos Islands, devastated by pine tortoise scale production. Seychelles scale (Icerya seychellarum) is a conspicuous pest as The endemic century plant (Agave the exclusion zone. We were fortunate to its body is covered with white and yellow missionum) has been almost wiped out have some highly experienced extension wax. It was observed to be widespread from most areas of the British Virgin workers, Elvis Gerald and Bernitta on crops (, breadfruit, citrus, Islands following the introduction of Serrant, show us some of their current guava and mango), ornamentals (palms), the agave snout weevil (Scyphophorus agricultural problems. Training was and more worryingly, on native plants in acupunctatus). A UKOT team from the provided to enable identification of the the Centre Hills (birch or copper wood Royal Botanic Gardens, Kew have been main groups of invertebrate plant pest and manceypot). Large populations cover working in collaboration with national and to diagnose plant damage. This the host plants with egested honeydew government bodies and other specialists capacity building will assist with detection which provides a medium for the growth to ensure the survival of these plants and of new pests. This is important as early of black sooty moulds, thereby reducing ecosystems. detection and identification of invasive photosynthesis and gas exchange. alien species can enable effective and Another recent introduction is the croton It is not only biodiversity that is affected, appropriate measures to be taken in a scale (Phalacrococcus howertoni) which the economy and human health can also timely manner to eradicate, contain was observed causing significant be seriously impacted by invasive alien and/or manage the pests. damage to ornamentals (croton) and species. The Asian pink hibiscus crops (mango, avocado, soursop and mealybug (Maconellicoccus hirsutus), Field work results sugar apple). This species is spreading which feeds on more than 330 plant rapidly across the Caribbean and will kill species, was introduced to the Caribbean More than 300 observations were made of croton plants if it is not managed. in the 1990s and caused huge economic invertebrates in Montserrat between 8th- losses until it was managed by the 16th November 2019. More than 150 introduction of a parasitic wasp and invertebrate species assigned to 4 classes, ladybird. Human health can clearly be 14 orders and 43 families were recorded. affected by the introduction of mosquitos Several species await identification (scale and the diseases they vector. insects and whitefly need to be slide- mounted), so the number of taxa recorded Biosecurity and Entomology will increase. Approximately 30 species, workshop in Montserrat including several invasive alien pests, were

A workshop organised by Jill Key of the GB Non-Native Species Secretariat, the Government of Montserrat and the author, with financial support from the UK Government Conflict, Stability and Security Fund was held in November 2019 to help strengthen biosecurity and protect their agriculture and natural environments. The workshop included field visits to ‘backyard farms’ to look for potential plant pests with staff from the Ministry of Agriculture, Lands, Housing and the Environment, and other workshop delegates. A huge range of edible plants are grown on Montserrat and in the past, the country even exported fruit and vegetables to neighbouring islands. Currently, the most productive agricultural land is no longer available as it occurs in The feeding damage of Lachnopus weevil (shown above) to Citrus

BGCI • 2020 • BGjournal • Vol 17 (1) 09

Some of the plant pests are host specific such as the avocado lace bug (Pseudacysta perseae), cassava scale (Aonidimytilus albus), fig whitefly (Singhiella simplex) and white cedar thrips (Holopothrips tabebuia); there are no prizes for guessing their host plants. While others are polyphagous (feeding on many different plant species), for example, a black weevil (Lachnopus sp.) was found causing serious damage to the foliage of many woody plants including avocado and citrus. There are at least 67 species of Lachnopus weevil recorded from the Caribbean, many of which are endemic to specific islands. Another example of a polyphagous pest is the A typical ‘Backyard’ farm in Brades illustrating the wide variety of vegetable crops and fruit trees that are coconut mealybug (Nipaecoccus nipae) commonly grown in Montserrat which was common on coconut, various ornamental palms and guava. The most very aggressive when guarding their Conclusion spectacular pest population observed nests, and won’t hesitate to sting; be consisted of about 50 giant Tetrio sphinx careful walking over grassy and disturbed The workshop was a great success with (Pseudosphinx tetrio) caterpillars (called areas as the red imported fire ant excellent participation by the delegates worms in the Caribbean), each up to 15 (Solenopsis invicta) nests are common and a remarkable number of plant pests cm long with striking black and yellow and are also very aggressive; and high- recorded over a brief period, largely due striped bodies, completely defoliating the heeled shoes are not suitable for field to local expertise. This baseline data is new growth on several frangipani plants. work (it wasn’t me wearing them). essential to be able to monitor any future changes in the fauna due to trade, Although many of the pests were The largest and most interesting tourism and climate change. abundant, there were also large numbers invertebrate observed was the endemic of beneficial predatory insects including Montserrat tarantula (Cyrtopholis Invasive alien species can have a huge ladybird beetles (ladybugs in the femoralis). It was found climbing a window impact on biodiversity, economy and Caribbean), lacewing larvae, assassin at a hotel behind Jill Key while she ate human health and islands are particularly bugs, social wasps, ants and hoverfly breakfast. She calmly rescued the giant vulnerable. The biodiversity and larvae. In addition, many of the scale spider by encouraging it to walk onto a unspoiled habitats in Montserrat are insects, whiteflies and psyllids were large seed pod and placing it safely in the globally important and need protecting. parasitized by chalcid wasps. hotel garden, while an audience of hotel This process is ongoing and Montserrat guests watched in admiration. has recently participated in a UKOT Some useful lessons were learnt by the Horizon Scanning workshop to identify delegates carrying out the field work My last observation on working in priority pest threats (run by the Centre for including: be careful when turning over Montserrat is that they have some of the Ecology & Hydrology, part of the large leaves as there may be a Jack loudest tree frogs croaking in the evening GBNNSS project ‘Tackling invasive non- Spaniard wasp (Polistes crinitus) nest that I have ever heard. I love the sound, native species in the UK Overseas attached to the underside. The adults are but others might need ear plugs to sleep. Territories’, funded by UK Government Conflict, Stability and Security Fund); and it has developed Pathway Action Plans to mitigate the risks.

Finally, I would like to express my gratitude to Jill Key (GBNNSS), staff from the Ministry of Agriculture, Lands, Housing and the Environment, and all the other delegates who attended the workshop. I was deeply impressed by their eagerness to participate, learn and actively ‘hunt bugs’ in the field.

All images credited to the author

Dr Chris Malumphy, Fera Science Ltd., Seychelles scale on mango Jack Spaniard wasp York, UK

BGCI • 2020 • BGjournal • Vol 17 (1) 10 FEATURE Author: Mira Fiskalović

FEATURED GARDEN BOTANICAL GARDEN “JEVREMOVAC”, BELGRADE, SERBIA

The Japanese Garden at the Botanical Garden ‘Jevremovac’, Belgrade (Kate Marfleet)

he first botanical garden in Serbia botanical garden in the schoolyard, even Garden. Unfortunately, the great scientist was founded in Belgrade in 1874, before the official garden was established, died in 1888, without having solved the Taffiliated to the Great School. for teaching and education activities. The problem of the location of the Garden. It was established at the proposal of first location for the garden, along the Josif Pančić, the destinguished Serbian banks of the Danube, was not suitable Knowing of Pančić’s problems, in 1889 King botanist and naturalist, and by the decree because of the possibility of flooding, Milan Obrenović donated his estate, inherited of the Ministry of Education of the which did actually happen twice. The two from his grandfather Master Jevrem, to the Principality of Serbia. Its first director great floods destroyed almost the entire Great School, for a botanical garden, under was Josif Pančić, Professor of Natural plant collection and Professor Pančić kept one condition – the Garden should be named Sciences, who was developing a small trying to find a better place for the after the King’s grandfather – Jevremovac.

BGCI • 2020 • BGjournal • Vol 17 (1) • 11-13 11 Ramonda nathalie Pančić & Petrović herbarium specimen from the Herbarium pancicianum (Snezana Vukojicic)

• plant propagation by tissue culture with special emphasis placed on the conservation of Serbian flora; • protection of rare and endangered plants of Serbia and the Balkan Peninsula.

The Garden spreads over 5 ha, with about 2,200 native, European and exotic species Collections inside the glasshouse of the Botanical Garden (Kate Marfleet) of trees, shrubs and herbaceous plants. It also includes two important collections – Soon after the transfer of the Garden to the • ecology of plant species and the Library and the Herbarium. new location, in 1892 the first greenhouse communities; was bought in Dresden, from the firm • studies of microorganisms and plants The Library Monzentin, and established in the Garden. as bioindicators of the environmental It was one of the largest and most beautiful state; Founded in 1853 at the Department of greenhouses in the Balkans. • development of microbiological assays Natural Sciences, the Library is one of the for the detection of genetic damage oldest and richest botanical libraries in In the decades to come, the Garden was caused by environmental agents; the region of southeastern Europe, with developed, reaching its peak in the 1930s, • identification of plant constiuents with more than 7,000 books. In its collection, under the guidance and leadership of the antimutagenic/anticancerous properties; there are many precious old, rare and revered botanist and academic Nedeljko • fundamental studies in plant physiology; exclusive editions. Košanin.

The Botanical Garden Jevremovac is today associated with the Institute of Botany. It is the teaching and scientific unit of the Faculty of Biology at the University of Belgrade, where over 1,200 students of regular and doctoral studies attend lectures dealing with algology, mycology and lichenology, microbiology, morphology and plant systematic, plant physiology as well as plant ecology and geography.

Teaching and scientific activities are realized through numerous projects and courses:

• plant and fungi taxonomic studies; • floristic and phytogeographic studies of The glasshouse was renovated and reopened for the visitors in 2014. Thanks to the financial support of the plant species of Serbia and the Balkans; European Union (Mira Fiskalović)

BGCI • 2020 • BGjournal • Vol 17 (1) 12 The oldest book in the library is The Natural History (L’ Histoire du Monde) by Pline the Elder, ancient Roman author and natural philosopher from the 1st century. Our copy is an old French translation, printed in Lyon in 1562. It is a luxurious edition, with leather binding, richly gold-tooled, with gilt edges.

The Herbarium

The Herbarium was established in 1860 by Professor Pančić, and today it is one of the oldest and richest in the region, with 200,000 sheets and over 300,000 samples of Balkan, European and world flora. The most precious segment is the personal herbarium of Josif Pančić, known as Herbarium pancicianum, consisting of 16,000 herbarium sheets.

The work of the garden

One the most important roles of botanical gardens nowdays is to participate in the protection and conservation of endangered plant species and the wider environment, through the education of both children and the adults, and actively through diverse projects.

The garden is involved in the ex-situ Ramonda nathalie Pančić & Petrović – example in ex situ conservation in the Botanical Garden (Snezana Vukojicic) protection of threatened plant species, covering about 20% of the total of 330 endangered plant species of Serbian In September 2019 we celebrated 130 internationally significant and critically vascular flora. Plants which cannot be years of work and existence of the easily grown ex-situ, are subjected to Botanical Garden Jevremovac and on that a special programme of tissue culture, occasion we hosted representatives of the by which hundreds of individuals are botanical gardens in neighboring countries developed from a single plant and made as well as representatives of BGCI. ready to be reintroduced back into nature. As well as being a green oasis in the centre of the capital city of the Republic The Parliament of the Republic of Serbia of Serbia, the Garden is a center of pronounced the Botanical Garden botanical research, a monument of both Jevremovac as a Natural Monument in nature and culture and an extraordinary 1995, due to its floristic richness and stage for diverse cultural manifestations, diversity. By this act the goverment exhibitions, concerts, theatrical plays, undertook the responsibility for its ballet performances and multicultural protection and development and put the events and spectacles. whole area of the Garden under a special regime. In 2007 the Garden was also Mira Fiskalović pronounced a Monument of Culture, due Institute of Botany and Botanical to its exceptional historical and cultural Garden “Jevremovac” heritage. University of Belgrade - Faculty of Biology In 2017 the Garden become a member of Takovska 43 BGCI. BGCI membership allows us not 11000 Belgrade, Serbia only to expand our knowledge and experience, but also to enrich our existing collections, create new ones and Collections inside the glasshouse of the Botanical work on species conservation to preserve Garden (Kate Marfleet) them for future generations.

BGCI • 2020 • BGjournal • Vol 17 (1) 13 FEATURE

INTERVIEW TALKING PLANTS

Is there anything our members can do to contribute/join in with IYPH?

You do not have to specialise in plant pathology to get involved with the IYPH 2020 and share its messages. The Food and Agriculture Organisation of the United Nations (FAO) and the International Plant For this issue of Protection Convention (IPPC) have BGjournal, with our produced a ‘getting started’ guide, focus on plant health, available on their dedicated IYPH website. we spoke to Professor The website has lots of information about Nicola Spence, Chief events being organised around the world, Plant Health Officer at and how people can get involved. Some the Department for suggestions include making a #Plant Environment, Food and Health commitment and sharing this on Rural Affairs, UK about the International social media, including messages about Year of Plant Health. plant health in outreach activities for children and members of the public, or Can you tell us a bit about the IYPH and organising your own IYPH event such as what it will involve? a concert, festival or tree planting event. One easy way to share the message of International Year of Plant Health (IYPH) in the IYPH is to update your web page with 2020 is a once in a lifetime opportunity to the IYPH button and link it to the IYPH raise global awareness on how protecting 2020 website. plant health can help end hunger, reduce poverty, protect the environment, and Why do you think botanic gardens are Why should we be worried about plant boost economic development. Events are important in terms of plant health? health? being organised around the world to celebrate IYPH and to highlight the vital Botanic gardens and arboreta are in a Plants make up 80 percent of the food role of national and regional plant health unique position to engage and enthuse we eat, and produce 98 percent of the organisations in protecting plants from their visitors about the importance of oxygen we breathe. Yet, they face damaging pests and diseases. practising good biosecurity. Many of continuous and increasing threat from these visitors will be plant enthusiasts pests and diseases on a global scale. UK events are being coordinated by and keen gardeners, therefore being the Moreover, international travel and trade a small team in the Department for ideal audience for messages about plant has tripled in volume in the last decade Environment Food and Rural Affairs health. Botanic gardens are able to set and can quickly spread pests and (Defra) alongside partners with an interest standards for the responsible sourcing diseases globally causing great damage in plant health. The UK focus of IYPH will of planting material, and many have to native plants and the environment. centre around a new national Plant Health been making a real effort to drive up Week, taking place from 20th to 27th standards in biosecurity in recent years. Every year, up to 40 percent of global food April 2020, and encompassing World Additionally, botanic gardens can join crops are lost to plant pests and diseases. Earth Day. It is hoped that this will BGCI’s International Plant Sentinel However, as the global population become an annual event thereafter, Network (IPSN), allowing their specimen continues to rise, and as many nations acting as a legacy of IYPH. collections to act as sentinels. Exotic become richer, it is predicted that plant species in certain gardens can be agricultural production must rise by 60 A number of conferences, workshops, used to predict which organisms are percent by 2050 in order to feed everyone. science outreach events and social likely to pose a threat in the sentinel’s It is therefore vitally important that we media campaigns are planned for IYPH native range in the future. The IPSN aims protect our plant and tree ecosystem 2020. Defra’s Plant Health Portal website for institutes to work together in order to from anything that can diminish its will provide further information on plans provide an early warning system of new health, damage our landscape and impact for IYPH in the UK. and emerging pest and pathogen risks. the economy.

BGCI • 2020 • BGjournal • Vol 17 (1) • 14-15 14 By not bringing in any plant material, everyone can play their part, alongside the actions of government and industry, by avoiding, unwittingly, bringing back something which may be infested or diseased.

One other simple measure that people can take to support plant health is to brush mud off footwear, bikes and buggies after visiting woodlands and parks. This can prevent the spread of potentially damaging pest and diseases that can be present in mud, water and leaves in outdoor environments.

What do you think are the top threats to global plant health?

Maintaining plant health in a changing climate is likely to become a global problem and the long-term effects of Barney Wilczak climate change on our crops and natural environments are unknown. Climate What do you think the most important What are some easy things people can do change is likely to influence the aspect of plant health will be for the next to support plant health? occurrence, prevalence, and severity of 5 years? many plant pests and diseases, affecting One of the most effective ways in which which crops are grown and how they are Encouraging companies and individuals people can support good biosecurity is managed. A major goal will be to protect, to source plants and plant products to avoid bringing any plants or seeds, manage and restore terrestrial and marine responsibly will be key to ensuring high , fruit or vegetables across environments to make them more resilient levels of biosecurity in the future. The borders after travelling abroad, as to the pressures of a changing climate. expansion of e-commerce in recent years highlighted by the recent “Don’t Risk It” has made it easier for many commodities campaign, jointly run by the Animal and Countries may have to adapt to changing to be rapidly sold and distributed across Plant Health Agency (APHA) and Defra. climates by diversifying the crops grown the world, including products potentially Pests and diseases can be present on and the different species planted in the posing a risk to plant health. These plants, seeds, flowers, fruit and natural environment, whilst following products are not always detected by vegetables, even if they look healthy, and strict biosecurity measures to help national plant protection organisations on soil clinging to the roots of plants or protect our landscapes from climate as they are sent in small quantities and on plant products, like root vegetables. change, pests and diseases. are not always correctly labelled. For example, seeds, which very often carry damaging viruses, can be easily bought Hyperlinks online and it is not always clear where these seeds originate or where they will World Earth Day - https://www.earthday.org/ be shipped from. Defra’s Plant Health Portal (IYPH page) - By purchasing trees, plants and seeds https://planthealthportal.defra.gov.uk/international-year-of-plant-health-2020/ from reputable nurseries and suppliers, and checking the product’s origin, you FAO IYPH ‘getting started’ guide - can be satisfied that these products have http://www.fao.org/documents/card/en/c/ca5188en been responsibly sourced and undergone the necessary checks to ensure that they IPSN - https://www.plantsentinel.org/ are of high health status. “Don’t Risk It” - https://www.gov.uk/government/news/public-urged-not-to- bring-plant-pests-and-disease-into-the-uk

BGCI • 2020 • BGjournal • Vol 17 (1) 15 ARTICLES

THE INTERNATIONAL PLANT SENTINEL NETWORK

WHAT ROLE CAN BOTANIC GARDENS AND ARBORETA PLAY IN UNDERSTANDING THE RISK THAT HARMFUL ORGANISMS POSE TO PLANT HEALTH?

THE BELGIAN PLANT SENTINEL NETWORK

THE GROWING ROLE OF BOTANIC GARDENS IN MITIGATING THE IMPACT OF INVASIVE ALIEN SPECIES

RISKS OF PEST AND DISEASE MOVEMENT VIA PLANT AND SEED EXCHANGES

ROSE ROSETTE VIRUS AND ITS POTENTIAL RISK

TRAP PLANTS AS PLANT SENTINELS

BIOSECURITY BEYOND QUARANTINE: THEMES FROM THE 2020 PLANT HEALTH ISSUE OF SIBBALDIA

BGCI • 2020 • BGjournal • Vol 17 (1) 16 ARTICLE Authors: Kate Marfleet and Suzanne Sharrock

THE INTERNATIONAL PLANT SENTINEL NETWORK

Agrilus planipennis (emerald ash borer); adult, an extreme close-up of the head capsule, showing all facial details. A specimen from Maryland, USA (Public Domain - Released by the United States Geological Survey (USGS)/USGS Bee Inventory and Monitoring Lab., Beltsville, Maryland, USA/via flickr)

not monitored. For example, the case of Sentinel plants can provide a way to Chestnut Blight (Cryphonectria parasitica) address this issue. They are individuals which was accidentally introduced into maintained outside of their native range the USA and devastated sweet chestnut and which can be monitored for attack by Background forests there in the first half of the pests and diseases which they wouldn’t twentieth century, despite being relatively normally encounter. Botanic gardens and lant pests and pathogens (referred harmless in Asia where it originated arboreta (BG&A) are a unique resource in to collectively as ‘pests’1) present a (Anagnostakis, 1987). For this reason the sentinel research for a number of reasons. Psignificant risk to global plant health majority of the most damaging alien pests They provide an incomparable source of and this threat is constantly evolving and that have or have had a dramatic impact curated plant specimens from a range of increasing due to the growing global trade on temperate forests would not have native and non-native species – often with of plant material and the impacts of been predicted as pests by conventional known provenance. It is estimated that climate change. A key issue in tackling methods for assessing plant health risks. 30% of known plant species are growing this threat is identifying future potential Predicting which pests are likely to in the living collections of BG&As, plant health risks. The majority of serious become an issue in the future is one of throughout the world (Mounce et al., 2017). invasive alien species are often not pests the greatest challenges in protecting Furthermore they employ knowledgeable, in their region of origin and are therefore global plant health. experienced and enthusiastic people,

BGCI • 2020 • BGjournal • Vol 17 (1) • 17-20 1 Pest: Any species, strain or biotype of plant, animal or pathogenic agent injurious 17 to plants or plant products issues amongst botanic gardens and arboreta (for first detection) and providing tools, such as posters and leaflets to aid early detection. Further, BGCI is working to build capability and capacity in botanic gardens and arboreta to support surveillance; encouraging monitoring for unknown threats, as well as known. The While the IPSN is at its heart a network IPSN provides training to staff in botanic of BG&As, the Euphresco partners have gardens and arboreta and develops expanded the network to include a materials to aid surveys and build broader range of research partners, knowledge. all contributing to sentinel research. By working together, the partners provide 2. Supporting Pest Risk Analysis (PRAs) access to an expanded pool of expertise, Impacts of Polyphagous Shot Hole Borer through research coordination and diagnostic services and funding. evidence gathering to address knowledge Supported by BGCI, Euphresco partners sometimes with access to diagnostic gaps to support PRA activities. This are helping to establish participation from capabilities; they have strong professional includes identifying research priorities and strong links to botanic gardens and international connections; and they have from NPPOs and RPPOs and coordinating arboreta within their own (and potentially access to informative international access to trusted botanic gardens and neighbouring) countries. databases. Monitoring these sentinel arboreta data, as well as coordinating the plants for damage by pests and pathogens activities of research partners, evaluation A number of articles in this issue provide not yet present in their native countries can and data sharing. Using BGCI’s unique reports on the activities of these provide vital information on potential future databases, and within the limitation of Euphresco partners (See Ronse et al. pest threats (Mansfield, 2019). data use agreements, the project can p. 24-26; Franić et al. p. 30-32 and produce maps showing the location of Starfinger p. 37-39). See Table 1 for The international network host species in gardens and pests a full list of Euphresco partners. present. Such maps are of value in PRAs The International Plant Sentinel Network and in prioritisation of the project’s Recent research activities: (IPSN) was established by BGCI in 2013. activities. It also involves energising The main objective of the IPSN is to act as participation and identifying research As described in the article by Lane and an early warning system, identifying new funding. This includes the coordination of Stevens (p. 21-23), in 2018, the IPSN UK and emerging pest risks. It aims to do this multi-country surveys for priority Research and Development committee by developing a network of interested organisms and host species using relevant identified three priority topics for further BG&A around the world, linked to plant botanic gardens and arboreta (in specific research to support PRAs. These topics protection scientists and National Plant countries/regions with particular host were selected on the basis of evidence Protection Organisations (NPPOs). The species) identified using BGCI’s unique gaps, suitability for research by network presently (January 2020) includes databases. A research survey to identify BG&A and potential for international 56 members located in 18 countries hosts of the meadow spittlebug which participation and collaboration. The around the world (www.plantsentinel.org). transmits the Xylella pathogen was carried research projects commenced in 2019. These gardens provide a first point-of- out in 2017 and a report of the results has contact for information on specific plant - been published. Further details of our The pests identified were: pest associations and are willing to carry research to support PRAs in the UK, as out surveys as requested by member identified by an IPSN Research and Gold spotted oak borer (Agrilus countries. The network acts on a Development committee, are provided in auroguttatus), Two Lined Chestnut reciprocal basis, with gardens, in the article by Lane and Stevens (p. 21-23) Borer (Agrilus bilineatus) and association with their NPPO, both and some results of our research projects Polyphagous Shot Hole Borer providing and requesting information on are described below. (Euwallacea whitfordiodendrus) on the impacts of pests and pathogens on European Quercus spp. These three specific host species growing outside their 3. Enhancing and expanding the wood-boring beetle pests have been native ranges and therefore exposed to network. The IPSN has been supported shown to cause significant damage to pests and pathogens they wouldn’t since 2013 by the UK’s Department for native US oak species. All three pests usually encounter. the Environment, Food and Rural Affairs have caused severe economic and (Defra) as a Euphresco (European environmental damage in the US, The network focuses on three main Phytosanitary Research Coordination) however their impact on European oak objectives: project. Euphresco is a network of species is so far undocumented. The organisations funding research projects IPSN is therefore carrying out a survey 1. Building capacity for the early and coordinating national research in of European oak species in US botanic detection of new and emerging pests the phytosanitary area. Phase 2 of the gardens to gain a better understanding and diseases, including known and IPSN was accepted as a three-year of the impact of these pests on unknown organisms. BGCI, through the Euphresco project in 2017, with BGCI European oak in order to inform IPSN is raising awareness of plant health providing the coordination. the UK risk register.

BGCI • 2020 • BGjournal • Vol 17 (1) 18 Institute Acronym Contact Activity

BGCI BGCI Katherine O’Donnell / • Coordination, capacity building, dissemination. Kate Marfleet / Suzanne Sharrock

Core Facility Botanical Garden, UNIVIE Michael Kiehn • Test options and identify problems for the detection and identification of potential pests and Faculty for Life Sciences, University invasive organisms. of Vienna, Austria • Bringing the Austrian network of botanical gardens into the project.

Agentschap Plantentuin Meise, APM Anne Ronse • Surveys and identification of emerging pests and selected pest organisms in Belgian Botanic Belgium Gardens and Arboreta, including laboratory testing by using molecular methods. • Face-to-face workshops for training garden staff and providing key networking opportunities. • Elaboration of a Belgian Plant Sentinel Network, integrated into the IPSN.

Central Institute for Supervising and UKZUZ Vladislav Rasovsky • Raising awareness of new phytosanitary risks. Testing in Agriculture, Czech • Developing a link between botanical gardens and diagnostic labs for diagnosis of new pests, Republic incl. a simple tool for this communication. • Surveys and monitoring of new and emerging pests in arboreta and botanical gardens in the Czech territory.

Julius Kuehn Institute, Federal JKI Uwe Starfinger • Further elaborate the ‘trap plant approach’ by refining protocols for choosing plant species, for Research Centre for Cultivated planting and for assessing damage. Plants, Germany

Consiglio per la ricerca in CREA Elisabetta Gargani / • Provide Italian botanic gardens and arboreta with information about new and emerging threats agricoltura e l'analisi dell'economia Sauro Simoni or susceptible host species. agrarian, Italy • Contribution to training material related to and nematodes.

Royal Botanic Gardens Edinburgh, RBGE Katherine Hayden • Risk assessment and sentinel research projects. Scotland

Animal Plant Health Inspection APHIS Heather Hartzog / • Provide expertise in risk analysis, pest data information management, and official pest Service, USA Heather Moylett reporting requirements.

University of Tuscia-DIBAF, Italy UNITUS Anna Maria Vettraino • Provide Italian botanic gardens and arboreta with information about new and emerging threats or susceptible host species. • Analysis of the structure of the fungal community of Pinus seeds from botanical gardens and/or arboreta in Europe and abroad.

Universitat de Lleida, Spain UdL Xavier Pons • Surveys in the Lleida’s Botanical Garden • Develop training material related to arthropods, and pest surveys in botanical gardens in its geographical area • Develop a Spanish Plant Sentinel Network.

Plant Health Australia PHA Greg Fraser • Access to the Virtual co-ordination Centre to the IPSN for collation and management of data

University of Copenhagen, Denmark UCPH Hans Peter Ravn • Provide an overview of knowledge on the fate of plants introduced to our botanical gardens and arboreta and identify specific information regarding establishment • Provide a list of native tree species for monitoring overseas.

AgResearch Limited, New Zealand B3 Mark McNeill • Identify overseas gardens and arboreta with New Zealand native plants. • NZ sentinel plants located in “hotspots” where severe plant pathogen or pest outbreaks are occurring. • Data on pest and pathogen incidence and impact from sentinel plant locations collected, collated and analysed. • Coordinate and facilitate links with Chinese researchers and botanic gardens. • Work with Chinese collaborators to access information published in Chinese of value to NZ biosecurity and conservation authorities. • Develop a project for one or more Chinese –speaking students who could work in a reciprocal way to survey and identify plant pests and conduct research projects.

Swedish University of Agricultural SLU Jonàs Oliva • Provide expertise in monitoring tree pathogens by the use of molecular methods. Sciences, Sweden

CABI (CH), Switzerland René Eschen • Database of pests and pathogens on selected tree species in botanical gardens, across Europe and continents. • Identify number of trees and locations (i.e. botanical gardens) that should be included in surveys to obtain a representative overview of pests on a tree species.

Table 1 provides a list of the partners included in the IPSN Euphresco project and their key activities.

BGCI • 2020 • BGjournal • Vol 17 (1) 19 Rose rosette virus (RRV) on Rosa spp. pest species, only PSHB was recorded. RRV is an emerging risk to rose It was found at four of the survey sites and cultivation. For more information, see the was shown to infest: Q. ilex, Q. robur and article by Franić et al in this issue (p. 30- Q. suber. An additional two gardens may 32). The IPSN is conducting a global have had either PSHB or the closely survey of rose collections in botanic related and indistinguishable Kuroshio shot gardens to assess the distribution of RRV hole borer (KSHB) Euwallacea kuroshio. outside of the known distribution area and establish whether the finding in India Rosa sp. survey: Survey forms and was an isolated case. posters were sent to a large number of gardens across Europe, Australia and Ash Dieback (Hymenoscyphus New Zealand. With the help of national fraxineus) and Emerald Ash Borer network coordinators, there was the (Agrilus plannipennis) on Chionanthus potential for over 700 gardens to have and Phillyrea spp. Ash Dieback is been contacted. So far 23 gardens have responsible for causing severe dieback on conducted surveys and none have found The Plant Health Checker (Kate Marfleet) ash species across Europe (including symptoms of RRV in their collections. Fraxinus excelsior and F. angustifolia). Acknowledgments Recently, H. fraxineus has been detected Chionanthus and Phillyrea sp. survey: on the non-Fraxinus hosts Phillyrea latifolia, A total of 93 BG&A were contacted with This work is funded by the UK’s P. angustifolia and Chionanthus virginicus the survey form and poster for these pests. Department for Environment, Food in isolated locations where H. fraxineus To date, 12 completed survey forms have and Rural Affairs (Defra) as part of the spore levels were high (Forest Research, been returned and a number of gardens Euphresco project: ‘An International 2019). This finding is the first non-ash host said they would participate but cannot Plant Sentinel Network as an early- record worldwide. The Emerald Ash Borer provide results until later in the year. warning system; research on future is a wood-boring beetle native to East Asia pest threats (IPSN II)’ which is currently causing significant Conclusion: damage to Fraxinus spp. in the USA and References Canada. In combination, these two threats The oak pest most likely to establish in are a serious concern for European ash Europe is PSHB with significant infection , Anagnostakis, S. L. 1987. Chestnut populations and the increased spread of found on Q. robur and Q. suber, both of Blight: the classical problem of an these through non-Fraxinus hosts is which are of high ecological, cultural and introduced pathogen. Mycologica, extremely concerning (Hill, 2018). The commercial significance. For the RRV 79: 23-37. doi:10.2307/3807741 IPSN is therefore conducting a survey to and Ash surveys, we believe more time assess whether any further findings of Ash and follow-up will result in more surveys , Forest Research. 2019. Chalara ash Dieback on Phillyrea and Chionanthus spp. being completed. The work conducted to dieback on different ash species and and Emerald Ash Borer on Chionanthus date will allow us to continue to collect non-ash hosts. Retrieved from virginicus have been recorded. data and feed this into PRA’s. https://www.forestresearch.gov.uk/new s/chalara-ash-dieback-different-ash- For each pest the main stages of the The plant collections of BG&A around the species-and-non-ash-hosts/ research project involved: world are an important resource, being used to support research, conservation , Hill, H. H. 2018. Maintaining 1. Mapping pest distribution against and education activities. In relation to ecosystem properties after loss of ash BG&A with host species of interest to plant health issues, monitoring plants in Great Britain. Journal of Applied identify target gardens growing outside their native regions Ecology, 56(2): 282-293. 2. Developing survey resources – posters, provides a valuable opportunity to doi:https://doi.org/10.1111/1365- survey materials and reporting increase our knowledge of new pest-host 2664.13255 mechanisms relationships. While the IPSN aims to 3. Contacting BG&A and issuing survey build on this and develop a global , Mansfield, M. A. 2019. The Value of resources community of BG&A focused on plant sentinel plants for risk assessment and 4. Compiling results and submitting a health issues, it is also clear that many surveillance to support biosecurity. preliminary report of our findings to UK botanic gardens are under-resourced and Neobiota, 48: 1-24. Risk Register scientists. lack the required expertise to carry out doi:10.3897/neobiota.48.34205 regular pest and disease monitoring and Results: surveying. However, as a networking , Mounce, R., Smith, P. and organisation, BGCI firmly believes that Brockington, S. 2017. Ex situ Quercus sp. survey: In total, 26 BG&A in these challenges can be overcome conservation of plant diversity in the the USA were contacted – 13 from through working together and sharing world’s botanic gardens. Nature Plants, California and 40 from the East Coast. experiences and information. We 3: 795-802 Survey forms were completed by 10 encourage interested gardens to consider Californian gardens and 4 East Coast joining the IPSN and becoming part of Kate Marfleet and Suzanne Sharrock gardens (though the East Coast Surveys our global effort to reduce the risk alien BGCI, 199 Kew Road, Richmond are still in progress). Of the three target invasive pests pose to our native floras. TW9 3BW UK

BGCI • 2020 • BGjournal • Vol 17 (1) 20 ARTICLE Authors: Charles Lane and Laura Stevens

WHAT ROLE CAN BOTANIC GARDENS AND ARBORETA PLAY IN UNDERSTANDING THE RISK THAT HARMFUL ORGANISMS POSE TO PLANT HEALTH?

Introduction scientific principles using pest risk introductions. Inevitably, there will always analysis (PRA) and based on international be areas of uncertainty in the assessment, rotecting the health of plants standards. These International Standards as scientific evidence may not be available is a difficult business; yet, on Phytosanitary Measures (ISPM) are at the time of assessment. This is Pthrough implementing good plant produced by the International Plant particularly pertinent when dealing with new biosecurity and international collaboration Protection Convention (IPPC); many or emerging plant pests or pathogens. The it is possible to mitigate against these of these standards provide the basic PRA will also include an assessment of risks. However, although we now all refer principles of phytosanitary measures (e.g. pest risk management options - again a to plant biosecurity what does it mean? ISPM 11: Pest risk analysis for regulated lack of scientific knowledge will result in Plant biosecurity can be defined as: quarantine pests) or more practical advice levels of uncertainty. ‘a series of precautions that aim to concerning the international movement prevent the introduction and spread of of plants, plant products or vehicles, Research and emerging threats harmful organisms’. This definition not machinery and equipment (e.g. ISPM 15: only refers to introduction and spread regulation of wood packaging material in A key role of the International Plant but also ‘harmful organisms’. Yet, with so international trade). Sentinel Network (IPSN) is to gather many organisms living in association with information to fill PRA evidence gaps. In plants, we need to identify which of these Pest risk analysis (PRA) is defined as: the UK, research priorities that could be should be considered as harmful (also ‘the process of evaluating biological or addressed by the IPSN are identified by referred to as a pest – including both other scientific and economic evidence to an R&D committee comprised of plant insects and pathogens) and able to determine whether an organism is a pest, health scientists, plant health threaten the health of a plant collection whether it should be regulated, and the policymakers and staff from botanic and of these, which may require strength of any phytosanitary measures to gardens and arboreta (BG&A). The co- regulatory plant health action? be taken against it’ (ISPM 5; Glossary). This design of these research projects ensures systematic process includes an evaluation they can be delivered by BG&A staff and The World Trade Organization (WTO) of hosts and pathways of introduction that they meet policy aims. Potential agreement on Sanitary and Phytosanitary and spread; life-cycle of the pest; it’s targets for research are drawn from the Measures (SPS) provides the framework epidemiology and sources of infestation, UK risk register, and other such pest risk for international plant health arrangements. and determine the relative economic, databases (e.g. EPPO Alert) as well as Phytosanitary measures must be based on environmental and social impacts of any information supplied by BGCI members.

BGCI • 2020 • BGjournal • Vol 17 (1) • 21-23 21 Other pests of concern, on a global scale, 1. Determining the risk of non-Fraxinus have included the brown marmorated hosts as a pathway of introduction for stink bug (Halyomorpha halys), that is the Emerald Ash Borer and Ash Dieback native to Asia, and has been accidentally introduced to other countries as a The Emerald Ash Borer is a wood-boring hitchhiker on containers, machinery and beetle native to East Asia, which is equipment. The bug is described as a currently causing significant damage to major agricultural pest affecting a wide- Fraxinus spp. in the USA and Canada. range of crops, and causes further With an estimated 100 million tree deaths problems when they overwinter in large being attributed to the pest which has numbers (often in the thousands) in resulted in serious economic damage as domestic and commercial structures. well as concern for the survival of several Colleagues in Australia and New Zealand, ash species and their associated where the pest is of considerable biodiversity. The beetle was also recently concern, have been able to share their recorded in a region of Moscow, Russia knowledge across the IPSN to help raise leading to serious concerns that it could awareness against this pest. Our work on spread to Europe. Emerald Ash Borer has Sirococcus blight is another example of also been shown to infest Chionanthus the IPSN’s role in sharing information virginicus in Ohio, the first record of about new and emerging pests and damage to a non-ash host. diseases. Sirococcos tsugae, is a damaging fungal pathogen, that causes Ash Dieback is responsible for causing shoot blight and cankers on cedar trees severe dieback on ash species across (Cedrus spp.) and shoot blight on Europe (including Fraxinus excelsior and hemlock (Tsuga spp.), attacking both F. angustifolia). It is caused by the The UK risk register (which now has more seedlings and saplings as well as mature invasive fungal pathogen than a thousand entries) identifies a trees. In the UK, it has caused major Hymenoscyphus fraxineus, causing subset of pests that have a priority for aesthetic damage to some iconic cedar crown dieback, lesions and the eventual research (approximately 40), but as a trees in public and private gardens. death of the tree. The disease was first dynamic database, new pests are added Information about this pathogen has been detected in Poland, but originated from on a regular basis providing further shared with IPSN members to help raise Asia, and has subsequently spread to opportunities for research. Looking at awareness about this disease worldwide. most European countries. Recently, H. these organisms, they include important fraxineus has been detected in a UK plant pests and pathogens such as acute The IPSN R&D committee has identified Arboretum on the non-Fraxinus hosts oak decline, Sirococcus tsugae and three priorities for research working with Phillyrea latifolia, P. angustifolia and Xylella fastidiosa. The latter of these BG&A around the world to gather Chionanthus virginicus in isolated poses an interesting challenge for the valuable information to inform pest risk locations where H. fraxineus spore levels IPSN. Possibly one of the most high- assessments. These are: were high. This finding is the first non-ash profile pathogens for many years and of host record worldwide. great concern to BG&A, the diversity of symptoms does not lend itself well to The IPSN is therefore conducting a BG&A-led research without diagnostic research project to assess whether there support. The general scorching dieback have been any further findings of both the of a wide range of plant material could be Emerald Ash borer on Chionanthus spp. easily confused with many other pests or and Ash Dieback on Phillyrea and pathogens, but also common cultural and Chionanthus spp. environmental problems. However, the IPSN has played an important role in 2. Understanding the distribution of raising awareness about this disease to Rose Rosette Virus to help identify BG&A and was able to assist in gathering introduction pathways evidence to fill a knowledge gap concerning vector hosts in the UK. Rose Rosette Virus (RRV) is an emerging risk to rose cultivation (See p. 33-36). It is A very successful social media-based present throughout the US and Canada survey #spittlebughunt collected valuable where it was described for the first time data from botanic gardens by asking in the 1940s. In 2017, the virus was found participants to take pictures of the in India, the first finding outside North characteristic ‘cuckoo spit’ on any named America. RRV is transmitted by grafting plants in collections. Although simple, it and by the mite Phyllocoptes fructiphilus. was highly effective and provided vital The mites are transported by the wind, by information to help remove some of the insects during pollination, and by contact uncertainty in the current PRA. Rose plant showing symptoms of RRV (Ines Vasquez) with clothes or gardening tools.

BGCI • 2020 • BGjournal • Vol 17 (1) 22 Quercus robur (Pixabay)

The symptoms include reddening of and crevices. Larvae burrow into the tree Conclusions newly emerged shoots, excess lateral and form feeding galleries under the bark. shoot growth and thorn production, These feeding galleries interrupt the Maintaining the health of a plant collection rosetting or witches’ broom, distortion of transport of food and water in the phloem is a challenging task, balancing the needs the leaves, malformations, mottling, and and eventually girdle individual branches to conserve the collection, whilst eventually plant death. Symptoms of the or the entire tree. They cause similar exchanging genetic material for virus are variable and depend on the damage to GSOB. Attacks occur in conservation and allowing visitors into the species or cultivar of rose affected, a stressed or dying oak (primary hosts) and collection. The movement of any plant diseased plant may only exhibit few of less frequently American chestnut. Live material can be risky as it provides an the above symptoms especially in the healthy trees are typically not infested. opportunity for the introduction or spread early stages of the disease. Attacks usually begin in the crown of the of plant pests and pathogens into the tree, with some branches dying in the collection. The same challenges are faced 3. Understanding the distribution and first year. Infestations gradually worsen, by national plant protection organisations damage caused by three emerging and the trees usually die in the second trying to protect the plant health of the pests to better understand the impact or third year. Incidence of attack by two region whilst needing to import food, and threat to Quercus species: lined chestnut borer increases following plants and plant products, and goods stress such as drought or defoliation from that may harbour pests. Phytosanitary Firstly, Goldspotted Oak Borer (GSOB), other pests. regulations and controls are in place to Agrilus auroguttatus, is a flat-headed mitigate against these risks and are buprestid (jewel beetle) that poses a And finally, Polyphagous Shot Hole Borer heavily reliant on international agreement major threat to oak trees. GSOB is native (PSHB), Euwallacea whitfordiodendrus, and collaboration. With scientific evidence to south-eastern Arizona, but was first is an invasive beetle that vectors three concerning these harmful organisms being recorded in California in 2004. GSOB fungi in the genera: Fusarium, Graphium fundamental to pest risk assessment to larvae feed beneath the bark damaging and Paracremonium. The adult female determine an appropriate level of the xylem and phloem as well as the tunnels galleries into a wide variety of protection, there is a great thirst for cambium. Trees die after several years of host trees, where it lays its eggs and knowledge. Research carried out in injury inflicted by multiple generations of inoculates the host with the fungi on botanic gardens and arboreta is helping the beetle, causing significant economic, which the beetle feeds. The Fusarium to fill these evidence gaps and reduce ecological, cultural, and aesthetic losses. fungus causes a disease called Fusarium uncertainty in pest risk assessments. GSOB poses a severe threat to Dieback (FD), which interrupts the susceptible oak species throughout transport of water and nutrients in over Dr Charles Lane California and elsewhere if it spreads. 110 tree species, which can kill the tree. Plant Health and Biosecurity Experts believe the beetles were Consultant, Secondly, Two Lined Chestnut Borer introduced into southern California via Fera Science Ltd, (TLCB), Agrilus bilineatus, is native to products and/or shipping material from York, UK North America; adults are recognizable as Southeast Asia. The PSHB/FD complex dark coloured buprestids with two golden has been found in other locations Dr Laura Stevens, stripes running lengthwise along their including Israel and South Africa. Plant Health Consultant, back. Females lay eggs in bark cracks Defra, UK

BGCI • 2020 • BGjournal • Vol 17 (1) 23 ARTICLE Authors: Anne Ronse, Hans Casteels, Anne Chandelier, Kris De Jonghe, Anne-Marie Deeren, Quentin Groom, Kurt Heungens, Martine Maes, Sophie Schmitz, Nicole Viaene

THE BELGIAN PLANT SENTINEL NETWORK

Practicing phytosanitary surveys with the PHC forms and taking samples in the botanical collections (BePSN)

Pest and disease surveys of Belgian botanic gardens and arboreta resulted The aims of the project were : in the first reports of two new tree pests in Belgium. - the creation of a sustainable Belgian network of BG&A and diagnostic labs Introduction: Agriculture, Fisheries and Food), partner of (NRL) for the survey and detection of the National Reference Laboratory (NRL) invasive pests and emergent diseases; he Belgian Plant Sentinel Network for Plant Health, because of a call for a - increasing the awareness and project ran for two years (16 April Belgian IPSN project. This was the starting knowledge of staff from BG&A to (new) T2017 to 15 April 2019) and was point for the elaboration of a national phytosanitary problems by trainings; funded by the Belgian Federal Public project with the participation of several - to implement and validate the protocols Service for Health, Food Chain Safety and botanic gardens and arboreta (BG&A). and tools developed by the IPSN for Environment. The official title was « the standardized data capture, and Belgian network and activities in the frame Organization and objectives development / validation of tools for of the International Plant Sentinel Network online data reporting. (Euphresco-IPSN2): BePSN ». The project The project partners were Meise BG was coordinated by A. Ronse, staff (MBG), as coordinator, and the Belgian These aims were translated into five work member of Meise BG (MBG, formerly NRL, consisting of ILVO and CRA-W packages:. (1) the general coordination and called National Botanic Garden of (Walloon Agricultural Research Center). management of the project, (2) capability Belgium). In 2016, she was contacted by In total, seven BG&A participated in the and capacity building, (3) phytosanitary ILVO (Flanders Research Institute for project, of which five were in Flanders surveys in the botanical collections and and two in Wallonia (in the northern and taking samples, (4) the diagnostic research the southern part of the country, and analysis of the samples, and (5) respectively; see Fig. 1) : outreach and dissemination.

• Agentschap Plantentuin Meise The scope of the surveys was limited to • Plantentuin UGent test cases, consisting of selected pests • Arboretum Bokrijk, Genk and diseases on targeted plant species. • Arboretum Robert Lenoir, Rendeux They were specifically chosen with the • Arboretum Wespelaar, Haacht aim of developing, testing and validating • Geografisch Arboretum van Tervuren the activities and performance of the • Parc et arboretum de Mariemont, network. This focus on test cases was Morlanwez. done because of the impossibility to survey all plants in the vast collections Furthermore, a Guidance Committee was of the BG&A within the restricted time Fig. 1: Botanic gardens and arboreta participating in established, composed of stakeholders horizon of the project, and because the the BePSN project (BePSN) as well as experts in the field. goal was not to generate large data sets.

BGCI • 2020 • BGjournal • Vol 17 (1) • 24-26 24 Fig. 2a and 2b:Information leaflet about survey test case of the root-knot nematode Meloidogyne mali (first page) (BePSN)

To make this selection, we concentrated Information leaflets about the test cases subsequently published in Zenodo, on topics and organisms: were drafted (FR/NL) and issued to the an online digital academic repository gardens (Fig. 2A and 2B). The Plant (Ronse, 2019). • that were in line with the target Health Checker (PHC) form was adapted organisms prioritized for IPSN2, yet to the survey test cases, and translated The Belgian project was presented at adapted to the Belgian situation; into Dutch and French (Fig. 3). Moreover, the launch of the second phase of the • with significant economic impact; a single PHC form was made for both international project (Euphresco-IPSN2) • for which limited background deciduous trees and conifers, combining during the 6th Global Botanic Gardens knowledge was available, but which the former separate forms. Finally, Congress in Geneva in June 2017. may have a major impact on plant electronic PHC forms were made in Similarly, a presentation about the health; Dutch/French/English using web forms in achievements of the project after one year • belonging to different taxonomic Google Drive, in order to facilitate data was given at the final meeting of the COST groups or disciplines: entomology, recording in the field using a smartphone action PP1401 “Sentinel plantings for mycology, nematology, virology and or tablet. detecting alien, potentially damaging tree bacteriology; pests” at Sursee (CH) in October 2018. • involving tree species largely present in More than 100 phytosanitary surveys There was regular communication with the the outdoor collections; were made by the BG&A, focusing on the IPSN secretariat in BGCI and participants • with varying degrees of specificity and test cases. Data were recorded using the to the transnational project by mailings, novelty. PHC, in either paper or electronic form, as well as by participation to the three and photographs of symptoms were international teleconferences organized The following test cases were selected by taken according to the IPSN guidelines. by the BGCI secretariat in 2018 and 2019. the partners of the Belgian project : The symptoms were screened, and The results and progress made in the a first-line alert and diagnosis was Belgian project were presented, and 1) Pine processionary moth performed by the gardens, based on opportunities for collaboration were Thaumetopoea pityocampa in conifers, the information obtained through the discussed. For the outreach to the general 2) The fungus Sirococcus tsugae in trainings and workshops. The diagnostic public, information about the project was cedars and hemlock (Cedrus spp., labs tested several methods for the put on the MBG website, and published in Tsuga spp.), identification of the targeted organisms, MUSA, the digital newsletter of MBG. In 3) Phytoplasma and root-knot nematode and adapted and validated them in order addition, weatherproof information panels occurrences in elm trees, to develop feasible detection methods. with illustrated texts about the project and 4) A general plant health survey on oaks They carried out a systematic campaign the issue of biosecurity were installed in (Quercus spp.). for on-site sampling in the collections of the two largest botanic gardens (Meise the gardens, especially for the apple and Ghent). They were discussed and approved at the root-knot nematode (Meloidogyne mali) International Plant Sentinel Network and Phytoplasma test cases. As a result, One of the aims of BePSN was the Workshop in Berlin on 10-13/10/2016, and two of the targeted organisms were establishment of a stable network, which were validated by the participating BG&A. recorded for the first time in Belgium could subsist in the long run and continue within this project: the phytoplasma to operate after the end of the period. A Activities and results ‘Candidatus Phytoplasma ulmi’ and the continuation of the network would ideally fungus Sirococcus tsugae. This resulted be via a new project with a coordinator, Several trainings were given for the BG&A, in the publication of two scientific but this would mean additional funding, with presentations of the project, available papers: De Jonghe et al. (2019) and for which the possibilities are restricted, tools and information sources, the survey Schmitz et al. (2018). Moreover, the although partial financing of the project test cases, guidelines for organising data obtained through the plant health could be realized through participation in surveys and sampling, including practical surveys by the participating gardens projects for status determination of pests demonstrations in the collections. were entered in a database, and were and diseases.

BGCI • 2020 • BGjournal • Vol 17 (1) 25 BG&A on phytosanitary issues, and increased the contacts with the diagnostic laboratories and with the governmental institutions competent in these matters. Plant health surveys were conducted with a standardized form, the Plant Health Checker, which was adapted and translated, and an electronic version was made and tested. This way of surveying is a novelty. In the context of this project, an active sampling campaign was done by the NRL for selected test cases, which led to first records for Belgium of two of the targeted organisms.

On the other hand, the active participation of each botanic garden or arboretum strongly depended upon their size and number of staff members, especially for Fig. 3: Dutch version of Plant Health Checker for conifers and deciduous trees (second page) (BePSN) making surveys. A prerequisite for surveying is also the presence of a good Finally, it was agreed that the best way , Ronse A. 2019. Plant health data from database of the collections, as well as for a lasting network would be to have it Belgian Plant Sentinel Network detailed maps of their location. Similarly, coordinated by the Belgian Association of [Dataset]. Zenodo. we found that there was a high threshold Botanic Gardens and Arboreta (VBTA; http://doi.org/10.5281/zenodo.2640894 for taking samples in the collections, as https://www.botanischetuinen.be/en). many gardeners were not familiar with the This is an active network of Belgian , Ronse A., Casteels H., Chandelier A., practice. In the course of the project, it BG&A, which regularly organizes De Jonghe K., Deeren A.-M., Groom Q., also appeared that most gardens are in meetings, trainings and other activities. Heungens K., Maes M., Schmitz S., need of more clarity about the procedures VBTA seems the most appropriate vehicle Viaene N. 2019. Belgian network and to follow in case of (new) phytosanitary for the perpetuation of the plant sentinel activities in the frame of the International issues, including the compulsory network, acting as the focal point where Plant Sentinel Network (Euphresco- notification and the possible all information on phytosanitary issues is IPSN2): BePSN. Final scientific report of consequences that are involved. brought together, and from where it is project RI 16/I-224 Be-PSN, funded by actively disseminated to the BG&A. This the FPS Health, Food Chain Safety and Through this project, it became clear that, would require regular contacts between Environment, Brussels, Belgium. because of their vast collections of exotic VBTA and the NRL, as well as the federal and native plant species, botanic gardens public services and federal agency for the , Ronse A., Casteels H., Chandelier A., can play a major role as sentinels for new safety of the food chain (FASFC) i.e. the De Jonghe K., Heungens K., Schmitz diseases and pests, and supply useful data Belgian NPPO (National Plant Protection S., Viaene N. & Maes M. 2018. One for Pest Risk Analyses, such as the host Organisation). year of Belgian Plant Sentinel Network range of pests. They can also provide (BePSN). In: Sentinel plantings for reciprocal information to other countries Scientific output detecting alien, potentially damaging about the occurrence of native disease and tree pests - State of the art 2018. pest organisms on species that are native , De Jonghe K., Deeren A.-M., Goedefroit COST Conference, 9–12 October to those countries or continents. Moreover, T. & Ronse A. 2019. First report of 2018, Sursee, Switzerland, Program they can spread information on ‘Candidatus Phytoplasma ulmi’ on elm and abstracts, p19. phytosanitary issues to the general public in Belgium. Plant Disease 103(7), 1763. through their contacts with a large number [http://dx.doi.org/10.1094/PDIS-12-18- , Schmitz S., Charlier A. & Chandelier A. of visitors, who are mostly interested in 2271-PDN] 2018. First report of Sirococcus tsugae plants and thus also inclined to introduce causing shoot blight on Cedrus atlantica plants from abroad. For these reasons, all , Ronse A. 2017. The Belgian Plant in Belgium. New Disease Reports 38: participants and stakeholders agreed that Sentinel Network (BePSN). In: 16. [http://dx.doi.org/10.5197/j.2044- a continuation of this network is important Abstracts of the BGCI 6th Global 0588.2018.038.016] and that in the future, Belgian status Botanic Gardens Congress, Geneva, projects for pest and disease organism 26-30 June 2017 (Eds. Loizeau P-A., Conclusions should include surveys in BG&A. Price M.J., Maeder A., Smith P. & Sharrock S.), pp. 138-139. The BePSN project has been successful Anne Ronse Conservatoire et Jardins Botaniques in bringing together a network of several Meise Botanic Garden de la ville de Genève, Publication Belgian botanic gardens and arboreta and Nieuwelaan 38 Hors-Série n°18, version 3. the National Reference Laboratory for B-1860 Meise doi:10.5281/zenodo.1158430 plant health. It raised the awareness in Belgium

BGCI • 2020 • BGjournal • Vol 17 (1) 26 ARTICLE Author: David AJ Teulon

THE GROWING ROLE OF BOTANIC GARDENS IN MITIGATING THE IMPACT OF INVASIVE ALIEN SPECIES1

Botanic gardens can make a tangible difference to mitigating the impact of IAS through biosecurity risk assessment, surveillance and awareness raising

Introduction

ew Zealand faces immense, insidious and often irreversible Neconomic, environmental and social impacts from Invasive Alien Species (IAS), including pests, diseases and weeds, to its valued productive and natural plant systems. Because of New Zealand’s economic reliance on primary production, and its unique flora and fauna, this country is especially vulnerable to IAS. New Zealand’s defence from IAS (i.e. border biosecurity) has been the top priority for its productive sector for the last 9 years (KPMG, 2019) and is a concern for many New Zealanders. Additionally, Biosecurity 2025 Strategic Direction 1 (1 of 5) “A Biosecurity Team of 4.7 Million” aims to make all New Zealanders aware of the importance of biosecurity and get them involved in pest and disease management (MPI, 2018). This article illustrates three areas where the New Zealand botanic community, and specifically botanical gardens, can make a difference to mitigate the impact of IAS.

New Zealand’s relative isolation has provided it with a natural advantage to exclude the many invasive alien species that attack valued plant and animal systems. However, like many countries the biosecurity challenges New Zealand faces are intensifying with changing trade, tourism and climate, and it needs to respond accordingly. Notwithstanding the reasonable claim that New Zealand has one of the best biosecurity systems in the world there will always be an ongoing need to do better. This article provides Visitors to the Auckland Botanic Gardens Biosecurity Trail can scan the QR code at each check point to be some examples where botanic gardens directed to either a video or website for additional information on the pest or the disease and how to prevent can make a tangible difference to its spread (Plant & Food Research) mitigating the impact of IAS.

BGCI • 2020 • BGjournal • Vol 17 (1) • 27-29 1 A version of this article has also been published in the Canterbury Botanical 27 Society Journal, New Zealand The New Zealand native/indigenous plant collection in the Royal Botanic Gardens Melbourne (Plant & Food Research)

Sentinel (expatriate) plants for example, is a project examining the gardens involved in this programme would biosecurity risk assessment status of myrtle rust on New Zealand have been beneficial in understanding the Myrtaceae in international gardens distribution of myrtle rust as it spread This concept is based on plant species (Marroni et al., 2018). Unfortunately, very throughout New Zealand (Fig. 1). being grown in foreign botanic gardens little useful information for biosecurity risk Auckland Botanic Gardens also hosts one or arboreta where these plants may be assessors was obtained from this study. of the many Ministry of Primary Industries exposed to pests and diseases they (MPI) High Risk Surveillance Sites where would not normally encounter. Better The sentinel plant concept works in the regular monitoring of plants occurs near Border Biosecurity (B3) has developed other direction as well, where New likely points of pest entry, such as airports, a database for international gardens Zealand botanic gardens can inform seaports and container devanning sites that contain significant planting of New other countries about the unique (Stevens, 2008). Zealand native/indigenous plant species pest/plant associations found here. (http://b3.net.nz/expat/view.php). Such an approach was taken by B3 and New Zealand botanic gardens have also Information from these novel pest/plant Christchurch Botanic Gardens researchers been involved in the development of a new interactions might then provide useful to assess novel pine aphid/conifer tree surveillance initiative in Australia to information on the potential damages interactions (Redlich et al., 2018). establish a programme of plant pest caused if these pest and diseases were surveillance within botanic gardens and to invade New Zealand. The sentinel/ The information gained from the sentinel arboreta (http://www.planthealthaustralia. expatriate approach can be particularly plant assessments must be treated with com.au/plant-pest-surveillance-in-botanic- useful for native/indigenous plants that some caution as foreign botanic gardens gardens/). This is intended to become part are predominantly grown in their native and arboreta will not necessarily reflect of the Australia National Surveillance range and have limited international the conditions or factors represented in Framework. Australia has over 150 botanic distribution and exposure to pests and the disease triangle, an established plant gardens and arboreta that are spread pathogens. B3 has been an international pathology paradigm, which is used to around Australia holding a range of native leader in the development of the explain plant disease interactions. The flora, exotic species and relatives of crop sentinel/expatriate plants concept host plant and plant pathogen factors are species, and are visited by millions of (Fagan et al., 2008, Mansfield et al., represented in foreign gardens but suitable people each year. 2019), is a founding member of The or comparable environment conditions for International Plant Sentinel Network disease expression may be absent. Biosecurity trail (IPSN) (https://www.plantsentinel.org/) maintaining a role on the IPSN Plant pest surveillance in A new walking trail developed by B3 at International Advisory Group. Botanic botanic gardens the Auckland Botanic Gardens provides gardens in Auckland, Wellington, an opportunity for local and overseas Christchurch and Dunedin are IPSN In New Zealand, the Auckland Botanic visitors to learn about New Zealand’s members. Gardens carried out some of the first flora as well as their potential role in (and thereafter regular and ongoing) protecting it. Visitors can embark on Perhaps the best example of this surveillance for myrtle rust starting in 2014 a 1.8-km walk around the garden and sentinel/expatriate approach is a study before this disease was found in New discover biosecurity facts at their own by Groenteman et al. (2015) examining Zealand. Following detection in New pace as they admire more than 10,000 the status of the plant pathogen Xylella Zealand, the main botanical gardens in native and exotic plants. Brief information fastidiosa and New Zealand indigenous Auckland, Wellington, Christchurch and about pests and diseases that threaten plant species in California. Important Dunedin all contributed to the national New Zealand’s flora and primary information was gained on the host surveillance programme for myrtle rust industries, including brown marmorated status of this plant pathogen on a range with additional data from a range of stink bug, myrtle rust and kauri dieback, of New Zealand indigenous plant alternative sources (Campbell et al., 2018). is displayed at each of the 12 check species. Another, but less successful There is no doubt that having more points along the path.

BGCI • 2020 • BGjournal • Vol 17 (1) 28 045 90 180 270 360 Data as of 6 August 2019 Kilometres !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! ! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! 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L.T., Bell, N.L., Kean, J.M., Barratt, Ministry of Primary Industries, Department of !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!! ^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!^!^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^!^!!!!!!!!!!!!!!!!!!^^^^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!^^^!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^^^^^^^^^^^^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! ^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^!^^^^^^^^^^^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^^^^^^!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!! Conservation, Plant and Food Research, ^^^^^^^!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! ^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^!^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^^!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! ! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! B.I.P., Boyd-Wilson, K., Teulon, D.A.J. Botanic Gardens, inaturalist (Myrtle rust reporter App, ^^^^^!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^^^^^^^^^^^ !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! ^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^^^! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! ^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^!!!!!!!!!!!!!!!! ^!!!!!!!!!!!!!!!!!!!!!!!!! ^^^!^^^!!!!! ^ !!! !!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!! !!!!! !!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! https://www.inaturalist.org/projects/myrtle-rust-reporter) !!!!!!!!!!!!!!!!!!!!!!!^ ! !!!!!!!!!!!!!!!! ! 2019. The value of sentinel plants !!!!!!!!!! ^! !!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! ! ! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!! ! ^^^^^^^^!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!! 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!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^^^!!!!! !!!!!!!!!!!!! ^^^^^^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^! !!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! for risk assessment and surveillance !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^^^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^^^!!!!!!!!^^^^^^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^!^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^!!!!!!!!!!!!!^^^^^^^^^^^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^^^^^^^^^^^^^^^^^^^^^^!!!!!!!!!^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^^^^^^^^^^^^^^^^^^^^^^^^^^^^^!!!!^^^^^^^^^^^^^^^! 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Map by Rebecca Campbell (Plant and ^^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!^^^^^^^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! ^ !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!^^^^^^^^^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !! ^^!!! !!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! to support biosecurity. NeoBiota 48: ^!!!!!!!!!^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !! ! !!!!!!!!!!!!!!! ! !!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! Food Research). To get your ^ !!! !!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!! ! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! ! !!!!! !!!!!! !!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! ^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! data on the map please contact ^!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! 1-24. !!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!! [email protected] !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!^^^^^^^^^^^!^^^^^^^^^^^^^^^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! ! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! ! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^^^^^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!! !!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^^^^^^^^^^^^^^^^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!^^^^^^^^^^^^^^^^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! , ^^^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^^^^!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!! Marroni, M.V., Boyd-Wilson, K., !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!! !!!!!!!! !!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! ^!!!!!!!!!!^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!^^^!!!!!!!!!!!!!!!!!!!!!!!!!!^!!!!!!^^^!!!!!!!!!!!!!!!!!!!!!!^^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^!!!^^^^^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^^^^^^^^^^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!! ^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^^^^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^^^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! ^^!^^!!!!!!!!!!!!!!!!!!!!!!!!!!!^!^^!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^ !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!! Campbell, R.E., McNeill, M.R., Teulon, !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! ! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! ! ^^^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! ^^^^^^^^^^^^^^^^ !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!! !!! !!! !!!!!!!!!!!!!!!!!!!!!!!!!!! ! !!! !!!!!!!!!!!!!!! !!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!! ! D.A.J. 2018. Location of overseas !!!!!!!!!!!!!!!!!! !!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!! ! !!!!!! !!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!! !!!!!!!!!!!!!!!!!!!!!!! botanic gardens with New Zealand !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! ^!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! ! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! ! Myrtaceae in relation to myrtle rust !!!!! ! !!!!!!!! !!!!!!!!!!!!!!!!!!!!!! !! !! !!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!! ^ MR finds in July 2019 occurrence. NZ Plant Protection 71: !! !!!! !! !!!! !!!!!!!!!!!!!!!!!!!!!!!!!!!!! !!!!! ^ MR finds before July 2019 356. doi: 10.30843/nzpp.2018.71.215. ! !!! !!! ! !!!!! MR searched for but not found in July 2019 ! !!!!! !! ! MR searched for but not found prior to July 2019 ! ! !!! , MPI. 2018. Biosecurity 2025. https:// ! ! www.biosecurity.govt.nz/protection- !!!! ! !!!!! ! !!!!!! and-response/biosecurity/biosecurity-2 !!!!!!!!!!!!!!!!!!!!!! !!!!! We would like to acknowledge the significant contribution !!!!!!!!!!! from staff at MPI and DOC who were involved in collecting, 025/. Accessed October 2019. !! !!!!!! compiling, anonymising and formatting the large amount of data since the beginning of the NZ MR response. This data !!!!!!!!!!!!!!!! We would like to acknowledge the significant contribution wasfrom criticalstaff at to MPI improving and DOC the who coverage were involved and quality in collecting, of data. , Redlich, S., Clemens, J., Bader, M.K- Diagnosticcompiling, anonymisingvalidations were and providedformatting by the plant large pathologists amount of atdata the since Plant the Health beginning and Environment of the NZ MR Laboratory response. (PHEL-MPI). This data F., Pendrigh, D., Perret-Gentil, A., was critical to improving the coverage and quality of data. Godsoe, W., Teulon, D.A.J., Diagnostic validations were provided by plant pathologists at the Plant Health and Environment Laboratory (PHEL-MPI). Brockerhoff, E.G. 2018. Identifying Fig 1. Myrtle rust distribution in August 2019. Four botanic gardens contributed surveillance data new associations between invasive (Plant & Food Research) aphids and Pinaceae (pines, spruces, firs) using plant sentinels in botanic Visitors can scan the QR code at each References gardens. Biological Invasions. DOI: check point to be directed to either 10.1007/s10530-018-1817-x a video or website for additional , Campbell, R.E. and Teulon, D.A.J. 2018. information on the pest or the disease Compiling myrtle rust surveillance data , Stevens, P.M. 2008. High risk site and how to prevent its spread. for the 2017-18 New Zealand incursion. surveillance (HRSS) – an example of NZ Plant Protection 71: 356. doi: best practice plant pest surveillance, While the trail will help raise the profile 10.30843/nzpp.2018.71.204. pp 127-134. In: Froud, K.J., Popay AI, of invasive pests and diseases with Zydenbos, S.M. eds., Surveillance for overseas visitors and the general public, , Fagan, L., Bithell, S., Fletcher, J., biosecurity: pre-border to pest aligned research on the trail will be used Cromey, M., Elder, S., Martin, N., Bell, N., management. Proceedings of a to improve New Zealand’s biosecurity Aalders, L., Cousins, K., Barratt, B., symposium held on 11 August 2008 in system. The insights that visitors gain on Ferguson, C., Kean, J., Phillips, C., Paihia, NZ. The NZ Plant Protection the Auckland Botanic Gardens Trail can McNeil, M., Barron, M., Dick, M., Kay, N., Society (Inc.), Hastings, NZ. be a significant way of engaging them Alcaraz, S., Kriticos, D. 2008. Evaluating with this important topic. the ‘Expatriate’ Plant concept: Can we David AJ Teulon predict invasive threats to New Zealand Director - Better Border Biosecurity The trail entered a 12-month trial period natural ecosystems by focussing our (http://b3nz.org/) in April 2019, during which time it will efforts overseas. Unpublished report. C/- The New Zealand Institute for continue to be improved on from the Better Border Biosecurity. Plant and Food Research Limited experience gained by feedback from Private Bag 4704 visitors. Information sheets in other major , Groenteman, R., Forgie, S.A., Hoddle, Christchurch, New Zealand languages, in addition to English, will M.S., Ward, D.F., Goeke, D.F., Anand, become available at this time. N. 2015. Assessing invasion threats: novel insect-pathogen-natural enemy Acknowledgements associations with native New Zealand plants in southern California. Biological Bec Stanley (Auckland Botanic Gardens) Invasions 17: 1299-1305. doi: and John Kean (AgResearch/B3) provided 10.1007/s10530-014-0804-0. useful comments to improve this document. Rebecca Campbell (Plant , KPMG. 2019. Agribusiness Agenda & Food Research/B3) produced Fig 1. 2019. https://home.kpmg/nz/en/home/ The Ministry for Primary Industries gave insights/2019/06/agribusiness-agenda- permission to publish the data in Fig 1. 2019.html [accessed September 2019.

BGCI • 2020 • BGjournal • Vol 17 (1) 29 ARTICLE Authors: Iva Franić, Eric Allan, Simone Prospero and René Eschen

RISKS OF PEST AND DISEASE MOVEMENT VIA PLANT AND SEED EXCHANGES

Seeds infested with larvae and blue fungi (Iva Franić)

Seeds and dormant twigs carry a large diversity of potentially pathogenic in importing countries and the extent of fungi and insects – vigilance when importing or exchanging plant material damage they can cause. As a result, these species were not targeted by phytosanitary is therefore highly recommended. measures. It would be important for the development and implementation of more effective plant protection measures that ive plants, including seeds, cuttings concern is not present, protection of the more harmful organisms are detected prior and potted plants, are moved around plants against pest and fungal infestation to their introduction. Lthe world on a large scale through at the place of production by means of trade and also as part of regular physical barriers, insecticide treatments Detection of potentially harmful organisms exchanges among botanic gardens. prior to export, border inspections and in countries of origin and the damage they This results in the movement of frequently import of plants during a season when may cause to important tree species in hidden plant-associated insect pests and pests are less likely to be associated importing countries can be done through microbial agents of diseases, which cause with the plants. surveys of organisms associated with important damage to trees in urban, “sentinel trees” that are planted for this agricultural and natural settings when they Plant protection measures largely target purpose, or that are present in botanic establish and attack trees in a new country. commodities that are considered of gardens, arboreta or parks. Surveying of particularly high risk and known pests. trees native to importing countries (i.e. Most countries perform risk assessment Lower risk commodities include seeds and exotic tree species where they are and implement phytosanitary measures deciduous plants without leaves. Most of surveyed) provides valuable and unique and procedures to reduce the risk of the pests and agent of diseases that have opportunities to detect damaging accidentally importing such harmful become established in recent decades organisms that are otherwise nearly organisms. Treatments, procedures and were not previously described, or species impossible to predict. Surveying of other conditions aimed at reducing the that were not known to be harmful prior commonly exported tree species has abundance of particularly harmful to their introduction to a new country or been shown to reveal many new host organisms on imported live plants include continent. For most species, it was associations that may be indicative of the production at places where the pest of unknown whether they can attack trees chance of introduction of those pests.

BGCI • 2020 • BGjournal • Vol 17 (1) • 30-32 30 pose a potential risk of establishment Fungi in dormant twigs in a new country because they can survive for a long periods in the seeds In another study, twigs of mature, and often do not need to mate to dormant trees were collected at 50 reproduce. Fungal diversity in seeds locations in 32 countries on all continents, was much higher than insect diversity, including botanic gardens, during the especially in angiosperm seeds which month after the shortest day. We focused contained around 50% of pathogenic on dormant trees because trees or fungi, in comparison with conifer species budwood are often traded in the season which contained around 30%. Both when deciduous species do not have traded and botanic garden seed lots leaves and foliar pathogens are less likely contained live fungi but it was found that to be introduced. Fungi were identified seeds from botanic gardens have higher using molecular tools from pooled, bark, fungal diversity than traded seeds with wood and needles/leaves of evergreen the overlap in fungal communities being species, and of bark, wood and buds around 50%. It is possible that this is of deciduous species. At each location, because traded seeds are obtained from samples were collected from one native managed forest stands and plantations, and up to three non-native congeneric The large diversity of fungi obtained from seeds and may even be treated before being tree species, of up to nine tree families (Iva Franić) distributed, while botanic gardens have of angiosperms and gymnosperms. higher plant diversity and normally no In a study led by CABI and the Federal treatments are used. Institute for Forest, Snow and Landscape Research WSL in Switzerland, funded by The combined results from the traded the Swiss National Science Foundation seeds and seeds from botanic gardens and related to COST Action Global suggest that seed-associated fungal Warning, we assessed the phytophagous communities are more host than site insects and fungi in tree seeds purchased specific. However, a certain degree from commercial suppliers and fungi in of geographic isolation of fungal tree seeds collected in botanic gardens communities was found, which suggests on two continents, as well as fungi and that further exchanges of seed material insects in dormant twigs from 32 could facilitate new introductions. countries to assess the diversity of such organisms and factors that may facilitate The results of this study suggest that their establishment in other countries. seeds pose a greater risk of pest introduction than previously thought, Fungi and insects in seeds but only a few species represent a real phytosanitary risk because these can be Seeds of eleven tree species native to transferred from the seed to the seedling. Europe, Northwestern USA and China More research is needed to gather data were obtained from commercial suppliers for better risk assessments. in Europe and the USA. Seeds of the same tree species were also obtained from botanic gardens in Europe and Northwestern USA. Each studied seed lot consisted of 100 seeds collected from a single tree species at a location. Seed insects were obtained from traded seeds by dissecting the seeds and fungi were grown on agar. Seed insects and fungi were both molecularly identified. Additionally, fungal communities were assessed molecularly directly from seed tissues obtained from trade and from ones collected in botanic gardens.

The number of insects in angiosperm seeds was lower than in conifer seeds probably in part because these insects leave the seeds to pupate in the soil. In the case of conifer species, many of the Above: Sampling for the global study in the Lushoto arboretum in Tanzania (René Eschen) seeds contained specialist insects that Top: Sampling for the global study in Hungary (Csaba Béla Eötvös)

BGCI • 2020 • BGjournal • Vol 17 (1) 31 A very large number of fungal taxa were new pests and diseases. Although identified and the fungal diversity in most particularly seed insects are highly host- tree families was highest around 45 specific, some of them are able to attack degrees latitude. Large differences in related tree species if these are present fungal communities were found in at their final destination. None of the samples from the different locations, with studied plant material showed external the fungal community in samples from signs of insect or fungal infestation, geographically close origins being more indicating that a healthy (asymptomatic) similar than those from more distant appearance by no means guarantees that locations. The fungal community was no harmful organisms are contained on or equally affected by the distance between within them. The absence of visible signs locations and the combined climatic of infestation highlights the need for factors (annual precipitation and careful surveillance of newly received temperature, and the amplitude of the material (quarantine) and good contacts average annual temperature range), with the local plant protection services. which appears to reflect differences in The chance of alternative hosts being climate among sampling locations and present is particularly high in botanic dispersal limitations of the fungi. Host gardens or arboreta and any seed lots identity was a comparatively much less and other planting material that have important factor in this study than it was been received from other collections in the two seed studies, which may should be kept in conditions that indicate that many of the fungi in this minimize the risk of insects escaping until study were horizontally transmitted, i.e. all insects have emerged. This may take the trees are infected by fungi present in more than one growing season, as the environment. The results from the especially conifer seed insects can stay seed studies were not as clear with in seeds for years, until the external regards to the origin of the fungi and it conditions become suitable. may be that the fungal community in Sampling for the global study in the Lushoto seeds is more affected by fungi Although our studies show that fungi arboretum in Tanzania (René Eschen) associated with the mother tree than associated with traded plant material are by spores in the air. very common, diverse and abundant, The invasion potential of fungal based on the current knowledge it is pathogens remains very difficult to Recommendations unlikely that many of them can be predict and vigilance when importing successfully transmitted to seedlings or or exchanging plant material is Our three studies show the diversity of mature trees and subsequently infect recommended. Surface sterilization of organisms that may be, or are carried on other trees or tree species. Some of the seeds prior to sowing may remove fungi plant material that is regularly exchanged well-known tree pathogens, such as on the seed coat. Furthermore, growing among botanic gardens or traded Fusarium circinatum, the causal agent trees in the greenhouse before planting commercially. Our results indicate that of pine pitch canker, however, have this them in the garden would allow closer movement of plant material is likely to capability and future studies may reveal surveillance to early detect pathogens. continue to facilitate the introduction of more cases of seed transmitted fungi. Similarly, frequent surveillance of newly planted trees may allow early detection of uncommon diseases, which greatly improves chances for eradication if that were necessary. In addition, monitoring of trees that are related to the imported species is of fundamental importance for detection of any new pests and diseases that attack new hosts in the collection.

Iva Franić1,2,3, Eric Allan2, Simone Prospero3 and René Eschen1

1 CABI, Delémont, Switzerland

2 Institute of Plant Sciences, University of Bern, Bern, Switzerland

3 Swiss Federal Institute for Forest, Snow and Landscape Research WSL, The large diversity of fungi obtained from seeds (Iva Franić) Birmensdorf, Switzerland,

BGCI • 2020 • BGjournal • Vol 17 (1) 32 ARTICLE Authors: Ines-Vazquez-Iglesias, Gerard Clover, Rebekah Robinson, Adrian Fox, Neil Boonham

ROSE ROSETTE VIRUS AND ITS POTENTIAL RISK

United States (US; Dobhal et al., 2016). Rose rosette virus (RRV) is the causal agent of this disease (Laney et al., 2011) and was first described in the 1940’s in Manitoba, Canada (Conners, 1941), later in Wyoming, and California (Thomas and Scott, 1953).

Host range

Rosa is the only host identified for RRV (Laney et al., 2011), although the susceptibility of different plant species has been evaluated. Rosa arkansana, R. bracteate, R. canina, R. corymbifera, R. gallica, R. glauca, R. multiflora, R. rubiginosa, R. spinossisima, R. villosa, and R. woodsii are all susceptible, including multiple types: climbers, hybrid teas, floribundas, miniatures, shrub and antique roses (Martin, 2014). RRV is distributed from the eastern coast of the US to the Rocky Mountains and California (Center for Invasive Species and Ecosystem Health, 2019). It was thought to be restricted to North America until 2017, when it was reported for the first time in India (Chakraborty et al., 2017).

Transmission

RRV is transmitted by the eriophyid mite Phyllocoptes fructiphilus (Keifer, 1966; Allington et al., 1968.), by grafting (Amrine Rosetting or witches’ broom caused by RRV (Ines-Vazquez-Iglesias) et al., 1988) and potentially by pollen (Babu et al., 2017a). Phyllocoptes Rose rosette virus threatens one of the world’s most beautiful and valuable fructiphilus is typically found in the angles between leaf petioles and axillary buds, ornamental plants feeding on the plant tissues and overwintering on plants. It is difficult to Introduction is around 18 billion cut stems, 60-80 identify these mites with the naked eye million potted roses and 220 million roses because of their small size (Druciarek et oses (Rosa L.) are one of the most for landscaping (Blom and Tsujita, 2003; al., 2016). Eriophyids do not have wings, valuable ornamental flowering Pemberton et al., 2003; Roberts et al., but they can be transported by insects Rshrubs and cut flowers grown 2003). during pollination, dispersed by the wind, worldwide, noted for their beauty and or by contact with clothing (Hong et al., scent, their desirable aesthetics, Roses are susceptible to infections 2012; Byrne et al., 2015). Further research landscaping and industrial properties caused by fungi, nematodes, bacteria, has been undertaken in other mite species (Dobhal et al., 2016). Cultivation of roses viruses and phytoplasmas. Rose rosette (e.g. P. adalius or Eriophyes eremus) to is economically important around the disease (RRD) is considered the most determine if they act as RRV vectors, but globe. The yearly estimated production important viral disease of roses in the as yet none have been identified.

BGCI • 2020 • BGjournal • Vol 17 (1) • 33-36 33 to 146 days after transmission of the varieties susceptible and resistant to the virus (Allington et al., 1968). Therefore, by virus and to the mite, with the aim to the time the first recognisable symptoms incorporate such traits into elite rose appear, the disease could have spread to germplasm (Byrne et al., 2015; Dobhal nearby plants (Hong et al., 2012). et al., 2016; Roundey et al., 2016).

Several diagnostic techniques have been Controlling the introduction of RRV and developed in the last few years. Nucleic its vector in the EU is needed to avoid a acid-based methods, including reverse high economic, environmental and social transcription-polymerase chain reaction impact. (Laney et al., 2011; Dobhal et al., 2016; Di Bello et al., 2017), RT-quantitative PCR (Arif Several pathways of introduction should and Ochoa-Corona, 2013), recombinase- be considered. Importation of infected polymerase amplification (Babu et al., plants is perhaps the most likely potential 2017a; Babu et al., 2017b) and loop- pathway. If infected plants were imported mediated isothermal amplification (LAMP) without the vector, the virus would be sequences (Salazar-Aguirre et al., 2016) limited to that plant, except if used for are currently in use. Non-targeted propagation (Tuffen, 2016). However, this methods, such as high throughput may be unlikely since plants showing sequencing are also used for RRV RRD symptoms are generally infested by detection (Peña-Zuñiga et al., 2017). P. fructiphilus (Otero-Colina et al., 2018). Jordan et al., (2018) recently developed Other less likely pathways are by natural polyclonal, monoclonal and/or single-chain spread or by the rosehip trade. Countries Reduced size caused by RRV antibodies and associated serology-based with RRV presence and P. fructiphilus are (Ines-Vazquez-Iglesias) protocols, such as enzyme-linked far from Europe, so vector transmission immunosorbent assay (ELISA). by wind is unlikely; and rosehips are Symptoms generally used for domestic consumption, Control therefore are unlikely to act as a pathway Symptoms of RRV include reddening on to the wider environment (Tuffen, 2016). newly emerging shoots, excessive lateral Identification and eradication of infected shoot growth, excess thorn production, plants and biosecurity measures are the RRV has not been reported infecting cut leaf mosaic and mottling, witches’ broom only current methods available to achieve rose varieties yet, although it is highly or resetting, and malformations (Laney et control (Hong et al., 2012). All susceptible probable that they are susceptible. The EU al., 2011). The virus moves throughout roses in a 100 m radius should be is a significant importer of fresh cut roses. the plant affecting roots, and plants show removed, because they serve as a source The possibility of finding cut flowers reduced growth and vigour (Epstein and of inoculum (Department for Environment, showing symptoms in the market is small Hill, 1999). Other symptoms include 2016). Pruning out symptomatic parts of since there is a high-quality standard for darkening of canes, short internodal plants is ineffective since the virus persists commercial flower production. distances, blind shoots, rough leaf in the root system (Di Bello et al., 2017). Nevertheless, flowers could be taken from texture and an increased susceptibility to asymptomatic parts of an infected plant. infections, especially by fungal diseases Complete elimination of the mite vectors Cut flowers are mostly used indoors, (Hong et al., 2012). Infected plants die by acaricide treatment is difficult, due to which reduces the risk of mites moving within 3-5 years of becoming infected their location in hidden areas of the plant outdoors to transmit the virus in gardens. (Di Bello et al., 2017). Symptoms of RRD (Otero-Colina et al., 2018). Acaricides However, when the cut flowers are vary depending on the type of rose may be useful to treat rose plants in disposed of outdoors, e.g. in compost, cultivars, stage of the disease and surrounding areas where RRV-infected mites may still be able to transmit the virus environmental factors (Epstein and Hill, plants have been removed or to decrease to other garden plants. The possibility of 1995; Epstein and Hill, 1999). mite populations, kill incoming mites and RRV being introduced by cut flowers is thereby reducing the risk of spread (Hong unlikely, but not impossible. Diagnosis et al., 2012). Economic impact Early detection is crucial for effective Resistant or immune rose cultivars are control of the disease. However, not yet available for RRD. The The economic impact is expected to be diagnosis of RRD in the early stages of development of new resistant varieties is high if RRV became established in Europe. infection is difficult. Symptoms are often a long process that takes several years. About 35% of shrub rose sales are confused with pest problems, herbicide Some species have shown levels of specifically for the landscape industry, and damage, nutrient deficiencies or fungal resistance to RRV infection, and others in the US this virus has led to a significant infections. Visual surveillance should be are resistant to feeding by the mite vector decline of garden roses for landscaping of used in conjunction with molecular or (Hong et al., 2012). Research groups in cities (Laney et al., 2011). Recently, this serological methods, either to confirm or the US are making efforts to develop market has been reducing the use of roses to assess the presence of the virus, as RRD-resistant roses: identifying genes by about 10% per year due to RRV and plants can remain asymptomatic for 30 linked to resistance, discriminating associated virus complexes.

BGCI • 2020 • BGjournal • Vol 17 (1) 34

Breeders, nurseries, landscapes, and plant material, to ensure infected material , Chakraborty, P., Das, S., Saha, B., retailers of garden and pot roses would is identified before the disease becomes Karmakar, A., Saha, D., Saha, A. 2017. also be affected. Symptomatic rose established. Long distance (between Rose rosette virus: An emerging plants would be unmarketable, and continents) vector spread is unlikely but pathogen of garden roses in India. eradication measures which include regulation of the movement of rose plants Australasian Plant Pathology 46, 223-6. destruction of roses within a range of between countries and awareness are 100 m, even if they remain asymptomatic, key to prevent the introduction of RRV. , Conners, L. 1941. Twentieth Annual would be damaging (EPPO, 2018). The Report of the Canadian Plant Report cost associated with replacement of rose Reference Survey, 1940. plants in private and public landscaping is high and the rose industry would be , Allington, W.B., Staples, R., Viehmeyer, , Department for Environment, Food and seriously affected by the introduction of G. 1968. Transmission of rose rosette Rural Affairs. 2016. Agriculture in the alternative ornamentals into both the by the eriophyid mite, Phyllocoptes United Kingdom 2015. National garden and landscape industry. fructiphilus. Journal of Economic Statistics. Countries such as Bulgaria and Turkey, Entomology 61, 1137-40. which are the largest producers of rose , Di Bello, P.L., Thekke-Veetil, T., oil worldwide, depend on species like R. , Amrine, J., Hindal, D., Stasny, T., Druciarek, T., Tzanetakis, I.E. 2017. damascena which is known to be an RRV Williams, R., Coffman, C. 1988. Transmission attributes and resistance host (EPPO, 2018). Transmission of the rose rosette disease to rose rosette virus. Plant Pathology agent to Rosa multiflora by Phyllocoptes 67, 499-504. Several European rose wild species are fructiphilus (Acari: Eriophyidae). susceptible to the virus, such as R. Entomological News 99, 239–52. , Dobhal, S., Olson, J.D., Arif, M., Garcia canina and R. rubiginosa (EPPO, 2018). Suarez, J.A., Ochoa-Corona, F.M. Roses are deliberately planted as , Arif, M., Ochoa-Corona, F.M. 2013. 2016. A simplified strategy for sensitive hedges, and for game cover, slope Comparative assessment of 5′ A/T-rich detection of rose rosette virus stabilisation and erosion control. overhang sequences with optimal and compatible with three RT-PCR Invertebrates that rely on Rosa spp. sub-optimal primers to increase PCR chemistries. Journal of Virological would also be affected, like the gall yields and sensitivity. Molecular Methods 232, 47-56. forming wasp Diplolepis spinosissimae. Biotechnology 55, 17-26. Pollinating insects may also be affected since rose flowers are a potential food , Babu, B., Washburn, B.K., Ertek, T.S. source (Tuffen, 2016). et al. 2017a. A field based detection method for rose rosette virus using The introduction of RRV to Europe would isothermal probe-based reverse cause serious social impact, from affecting transcription-recombinase polymerase the mental and physical health benefits amplification assay. Journal of associated with gardening (Soga et al., Virological Methods 247, 81-90. 2017) to loss of employment and income in the nursery and other sectors. The , Babu, B., Washburn, B.K., Miller, S.H. availability of rose products with cultural et al. 2017b. A rapid assay for importance like jam, rosehips, rose water, detection of rose rosette virus using rose petals of flower or buds is likely to be reverse transcription-recombinase reduced. More philosophically the rose is polymerase amplification using the national flower of England and other multiple gene targets. Journal of European countries, such as Bulgaria, the Virological Methods 240, 78-84. Czech Republic and Luxembourg. , Blom, T., Tsujita, M., 2003. Cut Rose Conclusions Production. In: Roberts, A., Debener, T., Gudin, S. eds. Encyclopedia of Rose is a valuable flower crop worldwide Rose Science. Amsterdam: Elservier and whilst it is affected by a range of Academic Press. pathogens, RRV is particularly devastating and could potentially be , Byrne, D.H,, Roundey, E., Klein, P., introduced and become established in Yan, M. 2015. Combating Rose Europe. Early detection and control Rosette Disease: Are there resistant programmes are necessary to avoid its roses? American Rose Society, USA introduction, establishment and spread. Visual assessment and the use of , Center for Invasive Species and serological and/or molecular methods Ecosystem Health. 2019. Rose rosette should be used for reliable diagnosis of https://roserosette.org/. Accessed Rosetting or witches’ broom in a dying rose stem infection in any suspicious, imported January 2019 (Ines-Vazquez-Iglesias)

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, Pemberton, H., Kelly, J., Ferare, J. 2003. Pot rose production. In: Roberts, A., Debener, T., Gudin, S. eds. Encyclopedia of Rose Science. Amsterdam: Elsevier Academic Press, 587-93.

, Peña-Zuñiga, L., Espindola, A.S., Klein, P. et al. 2017. EDNA-Rose a novel approach for detecting rose viruses combining next generation sequencing adn bioinformatics. Phytopathology 107: S5. 58.

, Roberts, A., Debener, T., Gudin, S. 2003. Introduction. In: Roberts, A., Debener, T., Gudin, S. eds. Encyclopedia of Rose Science. Amsterdam: Elsevier Academic Press, VI-VII.

, Roundey, E., Anderson, N., Bedard, C., Scheiber, M., Byrne, D.H. 2016. Evaluation of Rosa palustris as a parent for breeding rose rosette disease-resistant roses. Paper presented at the Ashs, Atlanta.

, Salazar-Aguirre, A., Molina-Cárdenas, S., Ochoa-Corona, F. O. 2016. Rose rosette virus detection using loop- mediated isothermal amplification (LAMP). Phytopathology 106: S4.117.

Malformation caused by RRV (Ines-Vazquez-Iglesias) , Soga, M., Gaston, K.J., Yamaura, Y. 2017. Gardening is beneficial for , Druciarek, T., Kozak, M., Maroufpoor, , Jordan, R., Guaragna, M.A., health: a meta-analysis. Preventive M., Lewandowski, M. 2016. Hammond, J. 2018. Development of Medicine Reports 5, 92-9. Morphological variability of Phyllocoptes polyclonal and monoclonal antibodies adalius female forms (Acari: to Rose rosette virus nucleoprotein. , Thomas, E., Scott, C. 1953. Rosette Eriophyoidea), with a supplementary Acta Horticulture 1193, 77-82. of rose. Phytopathology 43, 218-9. description of the species. 21, 181-94. , Keifer, H. 1966. Eriophyid Studies , Tuffen, M. 2016. Rapid pest risk , EPPO. 2018. Pest risk analysis for B-21. analysis (PRA) for: Rose rosette virus Rose rosette virus and its vector and its vector Phyllocoptes fructiphilus. Phyllocoptes fructiphilus. , Laney, A.G., Keller, K.E., Martin, R.R., Department for Environment, Food and Tzanetakis, I.E. 2011. A discovery 70 Rural Affairs (DEFRA). , Epstein, A., Hill, J. 1999. Status of rose years in the making: characterization rosette disease as a biological control of Rose rosette virus. Journal of Ines-Vazquez-Iglesias1,2, Gerard for Multiflora rose. Plant Disease 83, General Virology 92, 1727-32. Clover3, Rebekah Robinson3, Adrian 92-101. Fox1, Neil Boonham2. , Martin, C. 2014. Rose rosette disease , Epstein, A., Hill, J.H. 1995. The biology and the impacts on propagation. Acta 1 Fera Science Ltd., The National Agri- of rose rosette disease: a mite- Horticulturae, 319-21. Food Innovation Campus, Sand associated disease of uncertain Hutton, York, YO41 1LZ. aetiology. Journal of Phytopathology , Otero-Colina, G., Ochoa, R., Amrine 143, 353-60. Jr., J.W., Hammond, J., Jordan, R., 2 School of Natural and Environmental Bauchan, G.R. 2018. Eriophyoid mites Sciences, Agriculture Building, King’s , Hong, C., Hansen, M.A., Day, E. 2012. found on healthy and rose rosette Road, Newcastle upon Tyne, NE1 7RU. Rose rosette disease. Virginia State diseased roses in the United States. University Cooperative Extension, Journal of Environmental Horticulture 3 The Royal Horticultural Society, 450-620. 36, 146-53. Wisley, Woking, Surrey, GU23 6QB

BGCI • 2020 • BGjournal • Vol 17 (1) 36 ARTICLE Author: Uwe Starfinger

TRAP PLANTS AS PLANT SENTINELS

What are trap plants

t is a well-known practice in horticultural and agricultural systems to grow other Iplant species in addition to the desired crop. These “secondary plants” (Parolin et al., 2012) or “companion plants” can have various positive effects on the health and production of the main crop, e.g. by enhancing nutrient supply, by repelling or excluding pests and diseases or by attracting beneficial organisms. However, attracting pests can also be a useful function, either by retaining the trapped pest and avoiding damage on the desired plants or by indicating the presence of given pest species that are otherwise not visible (Parolin et al., 2012).

In this article, the term ‘trap plants’ is used to describe plants that trap pests and pathogens. Growing trap plants according to common protocols – Gazania and other spp. in the Julius Kühn Institut, History Braunschweig (EUPHRESCO Project IPSN I)

The use of trap plants to reduce insect Use of trap plants damage dates back centuries and is still used today in traditional farming systems For the trap plants to be effective it is and in organic farming (Hokkanen, 1991). important that they really act as a sink for Traditional examples include the use of the pest population and do not develop parsnip to trap and destroy parsnip into a source for new infestations. This webworms (Depressaria radiella) in carrot works for the rice striped stem borer Chilo farming (Curtis, 1860) or reducing the suppressalis attracted by vetiver grass impact of the parasitic broom rape (Vetiveria zizanioides) because the latter (Orobanche ramosa) on tomatoes by is a dead-end trap plant where larvae are trapping it on cowpea (Vigna sinensis) unable to complete their life cycle (Lu et and other plants (Qasem, 2019). In al., 2019). In other cases additional modern agriculture there are still a few techniques may be needed like crops in which this type of trap cropping vacuuming, sticky traps etc. (Holden et al., is successfully applied (Hokkanen, 1991). 2012). A specific example is the use of trap In sugar beet for example, trap plants can plants treated with an insecticide to attract Growing trap plants according to common protocols reduce the damage by cyst nematodes and kill insects, for example in cucumber – seedlings of Rudbeckia hirta (EUPHRESCO Project (Hemayati et al., 2017). and squash production (Pair, 1997). IPSN I)

BGCI • 2020 • BGjournal • Vol 17 (1) • 37-39 37 patria sentinel plantings in the sense of The use of trap plants can offer the same Eschen et al. (2019a). The idea to plant possibility as sentinel plants already plants for this purpose was developed in established, i.e. to monitor the the EU funded PRATIQUE project occurrence of known pests in an area (https://secure.fera.defra.gov.uk/pratique/ and to discover new pest-host relations. workPackages.cfm#WP1). Roques et al. Trap plants may however, have several (2015) planted European tree species in advantages: Chinese gardens and monitored the insect damage on these sentinel trees, while • They may be applied more flexibly over Vettraino et al. (2015) studied pathogens a given area, as the use of trap plants on them. Many pest species were found does not depend on already associated with the plants that were not established plants. previously known to attack them. The • New trap plantings may be initiated obvious disadvantage of using trees as from seeds rather than larger plants, Growing trap plants according to common protocols trap plants is their long lifespan and slow which can help overcome legal – Nolana napiformis in the Julius Kühn Institut, development, so for woody species, the restraints of cross-border transport Braunschweig (EUPHRESCO Project IPSN I) use of existing plantings instead of of plants for planting (Vettraino deliberately planting trap plants is often et al., 2019). Trap plants may provide an important tool preferred. Trap plants may also help in • The number of specimens of a given in protecting plants from pests that are commodity risk analyses, which species growing in botanic gardens currently spreading in Europe. A study in investigates the possibility that a traded and their genetic diversity is often the U.S. found that the brown marmorated plant from a given region can pose a limited so that the deliberate planting stink bug (Halyomorpha halys) is attracted phytosanitary risk. Kenis et al. (2018) of trap plants may be advantageous by sunflower (Helianthus annuus). There planted sentinel plants of species that are (Roques et al., 2015). In some cases, could be potential benefits of using exported from China in two different a broader genetic diversity may be sunflower as a trap plant in the production Chinese regions and found a high better to attract different strains of of bell peppers, but more research is percentage of pest-host combinations not a pathogen or specifically attractive needed before this can be applied previously known from the literature. clones or types of a trap plant can (Soergel et al., 2015). In the case of the be used. emerald ash borer (Agrilus planipennis), Conclusion: When is the planting • The propagation of trap plants girdled ash trees were effective in trapping of trap plants advisable? may follow detailed protocols so larvae and may therefore offer an element as to ensure that the plants have in strategies against the insect While research is continuing on a wide comparable attractiveness for the (McCullough et al., 2015). range of methods to detect new invasive studied pest or pathogen. pest species, the use of sentinel plants The use of trap plants is applied for enhancing biosecurity is now a widely These features together offer the preferentially for pests and pathogens accepted concept (Eschen et al. 2019b; possibility of conducting new vigorous that are small or hard to detect. For Mansfield et al. 2019; Morales-Rodriguez tests as they make the results example, airborne inoculum of pathogens et al. 2019). comparable over larger geographic areas. can be detected by physical traps, but trap plants are far more efficient in detecting them (Mahaffee & Stoll, 2016). Modern examples include the use of tomato plants for the indication of whitefly infestations in poinsettia (Euphorbia pulcherrima) crops (Parolin et al., 2012). Trap plants can also be used to monitor herbicide drift. In a 1996 study by Felsot et al., seedlings of pea, bean and corn (referred to as sentinel plants in this experiment) were used to detect such drift into nearby non-target areas.

Potential use for early detection of (new) pests and pathogens

In relation to the sentinel plant concept, the term trap plants can be used for plants that are specifically planted for attracting new pests (as opposed to those sentinel plants that already exist in botanic gardens Growing trap plants according to common protocols – Gazania and other spp. in the Botanic Garden of Potsdam or arboreta). As such, trap plants are ex- (EUPHRESCO Project IPSN I)

BGCI • 2020 • BGjournal • Vol 17 (1) 1FFH = Fauna-Flora-Habitat 38 , Hokkanen, H.M.T. 1991. Trap cropping , Pair, S.D. 1997. Evaluation of in pest management. Annu. Rev. systemically treated squash trap plants Entomol., 36:119–138 and attracticidal baits for early-season control of striped and spotted , Holden, M.H., Ellner, S.P., Lee, D.H., cucumber beetles (Coleoptera: Nyrop, J.P. and Sanderson, J.P. 2012, Chrysomelidae) and Squash Bug Designing an effective trap cropping (: Coreidae) in cucurbit strategy: the effects of attraction, crops, Journal of Economic retention and plant spatial distribution. Entomology, 90 (5): 1307–1314, Journal of Applied Ecology, 49: 715-722. https://doi.org/10.1093/jee/90.5.1307 doi:10.1111/j.1365-2664.2012.02137.x. , Parolin, P., Bresch, C., Desneux, N., , Kenis, M., Li, H., Fan, J.T., Courtial, B., Brun, R., Bout, A., Boll, R. and Poncet, Auger-Rozenberg, M.A., Yart, A., C. 2012. Secondary plants used in Eschen, R. and Roques, A., 2018. biological control: A review. Sentinel nurseries to assess the International Journal of Pest phytosanitary risks from insect pests Management, 58:2, 91-100, DOI: on importations of live plants. Scientific 10.1080/09670874.2012.659229. reports, 8(1): 1-8. , Qasem, J.R. 2019. Branched Growing trap plants according to common protocols , Lu, Y.H., Zheng, X.S. and Lu, Z.X. broomrape (Orobanche ramosa L.) – Schizanthus pinnatus damaged by unidentified 2019. Application of vetiver grass control in tomato (Lycopersicon pathogen in the Julius Kühn Institut, Braunschweig Vetiveria zizanioides: Poaceae (L.) as esculentum Mill.) by trap crops and (EUPHRESCO Project IPSN I) a trap plant for rice stem borer Chilo other plant species in rotation. Crop suppressalis: Crambidae (Walker) in Protection, 120: 75-83. https://doi.org/ Reference the paddy fields. Journal of Integrative 10.1016/j.cropro.2019.02.021. Agriculture, 18 (4): 797-804 DOI: , Curtis, J. 1860. Farm Insects. 10.1016/S2095-3119(18)62088-X. , Roques, A., Fan, J-t., Courtial, B., Glasgow, Scotland; Blackie & Son Zhang, Y-z.,Yart, A., Auger-Rozenberg, (quoted in Hokkanen, 1991 , Mahaffee, W.F. and Stoll, R. 2016. M-A., et al. 2015. Planting sentinel The ebb and flow of airborne European trees in eastern Asia as a , Eschen, R., O’Hanlon, R., Santini, pathogens: monitoring and use in novel method to identify potential A., Vannini, A., Roques, A., Kirichenko, disease management decisions. insect pest invaders. N. and Kenis, M. 2019a. Safeguarding Phytopathology,106 (5):420–431. PLoS ONE 10(5): e0120864. global plant health: the rise of sentinels. doi: 10.1094/phyto-02-16-0060-rvw. doi:10.1371/journal.pone.0120864. J. Pest Sci., 92:29–36. https://doi.org/ 10.1007/s10340-018-1041-6. , Mansfield, S., McNeill, M.R., Aalders, , Soergel, D., Ostiguy, N., Fleischer, S., L.T., Bell, N.L., Kean, J.M., Barratt, Troyer, R., Rajotte, E. and Krawczyk, , Eschen, R., De Groot, M., Glavendekić, B.I.P., Boyd-Wilson, K. and Teulon, G. 2015. Sunflower as a potential trap M., Lacković, N., Matosević, D., D.A.J. 2019. The value of sentinel plants crop of Halyomorpha halys (Hemiptera: Morales-Rodriguez, C., O Hanlon, R., for risk assessment and surveillance to Pentatomidae) in pepper fields. Oskay, F., Papazova, I., Prospero, S., support biosecurity. Neobiota, 48:1–24. Environmental entomology, 44. and Franić, I. 2019b. Spotting the pests https://doi.org/10.3897/neobiota. 10.1093/ee/nvv136. of tomorrow—Sampling designs for 48.34205. detection of species associations with , Vettraino, A., Roques, A., Yart, A., Fan, woody plants. J Biogeogr.; 46: 2159– , McCullough, D., Poland, T., and Lewis, J-t., Sun, J-h. and Vannini, A. 2015. 2173. https://doi.org/10.1111/jbi.13670 P. 2015. Lethal trap trees: A potential Sentinel Trees as a Tool to Forecast option for emerald ash borer (Agrilus Invasions of Alien Plant Pathogens. , Felsot, A.S., Bhatti, M.A., Mink, G.I. planipennis Fairmaire) management. PLoSONE 10(3): e0120571. and Reisenauer, G. 1996. Pest management science, 72. doi:10.1371/journal.pone.0120571 Biomonitoring with sentinel plants to 10.1002/ps.4083. assess exposure of nontarget crops to , Vettraino, A.M., Santini, A., Nikolov, C. atmospheric deposition of herbicide , Morales-Rodríguez, C., Anslan, S., et al. 2019. A worldwide perspective of residues. Environmental Toxicology Auger-Rozenberg, M-A. et al. 2019. the legislation and regulations governing and Chemistry, 15: 452-459. Forewarned is forearmed: harmonized sentinel plants. Biol Invasions. doi:10.1002/etc.5620150407. approaches for early detection of https://doi.org/10.1007/s10530-019- potentially invasive pests and 02098-3. , Hemayati, S.S., Akbar, M-R. J., Ghaemi, pathogens in sentinel plantings. A-R. et al. 2017. Efficiency of white NeoBiota, 47: 95-123. https://doi.org/ Uwe Starfinger, mustard and oilseed radish trap plants 10.3897/neobiota.47.34276. Julius Kühn Institute against sugar beet cyst nematode. Germany Applied Soil Ecology, 119: 192-196.

BGCI • 2020 • BGjournal • Vol 17 (1) 39 ARTICLE Author: Katherine Hayden

BIOSECURITY BEYOND QUARANTINE: THEMES FROM THE 2020 PLANT HEALTH ISSUE OF SIBBALDIA

Biosecurity notice at the entrance to the Royal Botanic Garden, Edinburgh (Ines-Vazquez-Iglesias)

he mission of botanic gardens and communities and highly managed In this article I summarise the themes arboreta (BGA) – to conserve plants systems (Antonovics and Hayden), the that emerged from this issue specifically Tby growing them outside their challenges that the climate emergency concerning biosecurity. These themes native habitats – presents a challenge and introduced and emerging pests1 and example strategies are outlined in for biosecurity. Harnessing what we know pose to BGA (Frediani; Saddler; Sharp Table 1; see the articles for explanation about novel species interactions can help et al.), the risks that pathogens pose to in greater detail. guide best practice. These themes were conservation horticulture (Frankel et al.; explored in a recent special issue of Green et al.; Summerell and Liew) and the While diseases are an important part of Sibbaldia, the journal of conservation approaches BGA are taking to learn from plant community dynamics, emerging horticulture published by RBGE. Articles (Marfleet and Sharrock) and mitigate diseases caused by invasive non-native in this issue outline the peculiar space them (Hayden; Ives; Marfleet and pests (INNP) present a grave threat to BGA occupy between ‘natural’ plant Sharrock; Summerell and Liew). collections and to species at risk.

BGCI • 2020 • BGjournal • Vol 17 (1) • 40-42 1 Defined broadly to mean any disease-causing organism 40 Goal Mitigation Example techniques

Preventing arrival of • Sourcing & importing • Sourcing by seed if possible and only from healthy plants, new pests with procedures cleaning away soil or growing media before importing collections • Inspection procedures • Accept only healthy propagules; inspect at least on intake and • Quarantine procedures end of quarantine period • Seclusion period for all plant material on intake. Longer length and higher security for high risk and international origin

Reducing opportunities • Biosecurity procedures in • Limited access, foot and hand sanitation on entry and exit, for growth and propagation elevating plants, organising workflows to reduce contamination transmission of • Biosecurity procedures in • Cleaning tools and shoes, avoiding unnecessary soil disturbance established pests, living collection or spread, separating unfinished compost from collection whether invasive or • Monitoring signs and • Regular condition checks, IPSN plant checker, surveys in endemic symptoms of disease propagation areas. Staff training, culture to protect collection as • Monitoring pests well as individual accessions independent of disease • Insect traps, bioassays or DNA-based monitoring for cryptic pests • Cultural practice like Phytophthora spp. • Curating for diversity • Removing and safely disposing diseased material, maintaining • Visitor procedures drainage, pruning canopies to maintain airflow and keep above soil level • Where possible avoid large groupings of a single species • Sanitising visitor footwear; education and outreach

Reducing risk of • Procedures to reduce pest • All of the above transmission from living prevalence in collections • Rigorous visual inspection; DNA-based screens or bioassays for collections to the • Procedures for inspection cryptic pathogens environment before dispatch • Sanitising vehicles, equipment, shoes, tools before leaving home • Hygiene during and between sites; minimising soil movement; beginning work translocation in areas least likely to be contaminated before moving to higher risk sites

Table 1. Biosecurity goals, mitigation measures to achieve those, and some example techniques employed by BGA. Table compiled from articles in the 2020 Sibbaldia Plant Health Issue. For greater detail see especially Frankel et al.; Frediani; Hayden; and Summerell & Liew.

Emerging diseases in collections and for inspection and quarantine of threaten specimens directly and through incoming plant material, beyond what destruction as a part of eradication efforts, is required by national and international while additional mortality can put extreme statutes. Sourcing procedures can help pressure on populations already under to reduce the risk that material carries stress, as are many of the species targeted pests, whether from the wild, from other for conservation (Frankel et al.; Summerell collections, or from commercial sources. and Liew). BGA may harbour more The risk of latent pathogens is never zero, pathogens than they realise: Phytophthora so some kind of quarantine period for incidence and diversity in soils in BGA is all incoming plants, with the type remarkably high (Green et al.), and can determined by relative risk of plant spill over to new hosts in collections and material type and its origin. through translocations (Frankel et al.; Symptoms of Ash Dieback Hayden; Summerell and Liew). From the second point follows a call to reduce pest populations and With this view, biosecurity in BGA can be opportunities for transmission in seen to follow two organising principles: propagation nurseries and living 1. Pests are most dangerous to plants collections. A successful pest must when they establish outside of their co- transmit itself to at least one host for evolved systems (e.g. in naive hosts in a each one it infects; less than that and it new geographic area) and 2. The larger will die out. Thus biosecurity in BGA is the pest population, the larger the chance not just to prevent pests from arriving: of transmission and disease emergence good biosecurity practices reduce the in new hosts and new localities (Table 1). opportunities for transmission of pests Limited access in plant propagation areas and that have already arrived, whether native sanitation for footwear are biosecurity measures help From the first point follows a need to or new arrivals. In turn, this both reduces prevent new pests from establishing and reduce reduce the risks of importing new pests direct threats to the collection from these transmission rates and population sizes of pests that with new collections. This is primarily pests, and reduces the chance of a new have already arrived. addressed with procedures for sourcing epidemic originating from the collection.

BGCI • 2020 • BGjournal • Vol 17 (1) 41 conservation nurseries into the environment have shown (Frankel et al.), translocating plants to sensitive environments requires extra care (Hayden; Summerell and Liew).

Conclusion

Biosecurity in BGA is of increasing importance, and goes beyond keeping new pests out of our collections. Actions to reduce the opportunities for adaptation Only a single tree remained in the source population, and emergence of pests –primarily by so to help augment it rooted cuttings of A. argotaenia reducing their numbers – are a key part were sent from RBGE to Kadoorie Farm & Botanic of conservation horticulture, and are Garden in Hong Kong. Cuttings were transplanted necessary to protect threatened species into inorganic media prior to shipment to reduce the within and outside collections. risk of accidentally transporting pathogens in soil. Amentotaxus argotaenia in collection at RBGE Acknowledgements , Marfleet, K., and Sharrock, S. 2020. Large-scale production systems create The International Plant Sentinel an opportunity for pathogen populations This work is funded by the Scottish Network: an update on phase 2. to grow large and diverse enough to Government SEFARI Responsive Sibbaldia 18:105–116. beat the odds against adapting to Opportunity Initiative, the players of the new environments, and to overcome People’s Postcode Lottery UK, and as , Saddler, G.E. 2020. An integrated resistance in normally non-susceptible part of the Euphresco project ‘An approach to meet future plant health hosts. The relatively small size and high International Plant Sentinel Network as challenges in Scotland. Sibbaldia 18, plant diversity of most BGA is helpful, an early-warning system; research on 141–145. because while intensive production future pest threats (IPSN II)’. favours large pest populations and , Sharp, L., Hurst, C., Drakulic, J., and fosters adaptation, host diversity can Reference Cromey, M. 2020. Environmental help prevent pest epidemics, reducing influences on box blight epidemics. the number of susceptible hosts and , Antonovics, J., and Hayden, K. 2020. Sibbaldia 18:37–51. by increasing the complexity of the Global hosts and global pathogens: environment to which pests must adapt. a perspective. Sibbaldia 18: 5–17. , Summerell, B.A., and Liew, E.C.Y. These factors all help to reduce risk that 2020. Phytophthora root rot: its impact new pathogens establish in BGA. , Frankel, S.J., Alexander, J., Benner, in botanic gardens and on threatened However, this reduction is offset by the D., Hillman, J., and Shor, A. 2020. species conservation. Sibbaldia 18: frequency and distance of trade among Phytophthora pathogens threaten rare 89–104. them, which increases risk, and the habitats and conservation plantings. increased opportunity for new host Sibbaldia 18: 53–65. Katherine Hayden relationships (Antonovics and Hayden). Royal Botanic Garden Edinburgh Biosecurity within collections is thus , Frediani, K.L. 2020. Inverewe: gardening Scotland, EH3 5LR UK called for to reduce i) the likelihood that on the edge. Sibbaldia 18: 19–35. a newly introduced pest becomes established; ii) the likelihood that a more , Green, S., Riddell, C.E., Frederickson- aggressive or damaging pest will arise Matika, D., Armstrong, A., Elliot, M., out of an established population through Forster, J., Hedley, P.E., Morris, J., adaptation and/or hybridisation; and iii) Thorpe, P., Cooke, D.E.L., et al. 2020. the likelihood that endemic pests will Diversity of woody-host infecting reach epidemic numbers. Phytophthora species in public parks and botanic gardens as revealed by From both points follows a call to reduce metabarcoding, and opportunities for the risk of transmission from living mitigation through best practice. collections to the environment. This is Sibbaldia 18: 67–88. especially important when plants from ex situ collections are used to re-establish , Hayden, K. (2020). Botanic gardens or augment wild populations. These and plant pathogens: a risk-based risks are necessarily reduced when the approach at the Royal Botanic Garden Water runoff from the cuttings was tested for cryptic opportunities for contamination and Edinburgh. Sibbaldia 18: 127–139. pathogens using pears as a bioassay. Once a ‘clean’ transmission within the collection and result was returned from bioassays, phytosanitary propagation facilities are lowered, as , Ives, J. (2020). Biological controls in inspections were performed by the national plant above, but as significant escapes from botanic gardens. Sibbaldia 18: 117–125. protection organisation and the plants were shipped.

BGCI • 2020 • BGjournal • Vol 17 (1) 42 Plants matter.

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