Journal of Botanic Gardens Conservation International

Volume 8 • Number 2 • July 2011

Botanic gardens and invasive alien species Volume 8 • Number 2 EDITORIAL SARA OLDFIELD 02

EDITORS

03 23 BUILDING AN INTERNATIONAL CODES OF CONDUCT TO Suzanne Sharrock Sara Oldfield SENTINEL NETWORK REDUCE THE THREAT OF Director of Global Secretary General Programmes ANDREA KRAMER AND ABBY HIRD INVASIVE SPECIES INTRODUCTION AND SPREAD Cover Photo : Impact of Emerald Ash Borer on a stand of Ash trees in the USA (Andrew Gapinski) THROUGH BOTANIC GARDENS

Design : John Morgan, Seascape SARAH REICHARD www.seascapedesign.co.uk

BGjournal is published by Botanic Gardens Conservation International (BGCI) . It is published twice a year and is sent to all BGCI members. Membership is open to all interested individuals, institutions and organisations that support the aims of BGCI (see inside back cover for Membership application form). Further details available from: 07 • Botanic Gardens Conservation International, Descanso House, 199 Kew Road, Richmond, Surrey TW9 3BW BIOSECURITY – ROYAL BOTANIC UK. Tel: +44 (0)20 8332 5953, Fax: +44 (0)20 8332 5956 GARDENS MELBOURNE E-mail: [email protected], www.bgci.org PETER SYMES • BGCI-Russia, c/o Main Botanical Gardens, Botanicheskaya st., 4, Moscow 127276, Russia. Tel: +7 (095) 219 6160 / 5377, Fax: +7 (095) 218 0525, E-mail: [email protected], www.bgci.ru • BGCI-Netherlands, c/o Delft University of Technology 26 Julianalaan 67, NL-2628 BC Delft, Netherlands Tel: +31 15 278 4714 Fax: +31 15 278 2355 A CODE OF CONDUCT ON E-mail: [email protected] www.botanischetuin.tudelft.nl INVASIVE ALIEN SPECIES FOR • BGCI-Canarias, c/o Jardín Botánico Canario Viera y Clavijo, ’S BOTANIC GARDENS Apartado de Correos 14, Tafira Alta 35017, VERNON H. HEYWOOD Las Palmas de Gran Canaria, Gran Canaria, Spain. Tel: +34 928 21 95 80/82/83, Fax: +34 928 21 95 81, E-mail: [email protected] • BGCI-China, 723 Xingke Rd., Guangzhou 510650 China. 14 Tel:(86)20-37252692. email: [email protected] www.bgci.org/china PREVENTING AND MANAGING • BGCI-Colombia, c/o Jardín Botánico de Bogotá, PLANT INVASIONS ON OCEANIC Jose Celestino Mutis, Av. No. 61-13 – A.A. 59887, ISLANDS Santa Fe de Bogotá, D.C., Colombia. Tel: +57 630 0949, Fax: +57 630 5075, E-mail: [email protected], CHRISTOPH KUEFFER www.humboldt.org.co/jardinesdecolombia/html/la_red.htm • BGCI(US) Inc, c/o Chicago Botanic Garden, 1000 Lake Cook Road, Glencoe, Illinois 60022, USA. E-mail: [email protected], www.bgci.org/usa BGCI is a worldwide membership organisation established in 1987. Its mission is to mobilise botanic gardens and engage partners in securing plant diversity for the well-being of 29 people and the planet . BGCI is an independent organisation registered in the United Kingdom as a charity (Charity Reg No USEFUL BUT POTENTIALLY 1098834) and a company limited by guarantee, No 4673175. BGCI is a tax-exempt 501(c)(3) non-profit organisation in the INVASIVE IN THE USA and is a registered non-profit organisation in Russia. MEDITERRANEAN REGION: Opinions expressed in this publication do not necessarily 18 reflect the views of the Boards or staff of BGCI or of its WHAT RESTRICTIONS SHOULD members THE REASONS FOR BE PLACED ON THEIR USE IN EXOTIC PLANT INVASIONS GARDENS? AND WHY BOTANIC GARDENS OLIVIER FILIPPI AND JAMES ARE PARTICULARLY ARONSON VULNERABLE QUENTIN J. GROOM, ANNE RESOURCES 34 RONSE AND IVAN HOSTE

BGCI • 2011 • BGjournal • Vol 8 (2) 01 EDITORIAL: Tackling invasive species

ackling invasive species is a major global challenge. The CBD’s TStrategic Plan for Biodiversity 2011-2020 recognises that the impact of invasive species is one of the main underlying causes of biodiversity loss and has set a specific target that: By 2020, invasive alien species and pathways are identified and prioritised, priority species are controlled or eradicated, and measures are in place to manage pathways to prevent their introduction and establishment . Botanic gardens and our networks are well placed to help implement this target and the related Target 10 of the GSPC. With the long tradition of growing introduced species, botanic gardens can and do test invasiveness and help identify the pathways of invasive species. Botanic gardens are also frequently involved in species will be incorporated into the Managing natural areas that have been the eradication of invasive species both updated version of the International invaded by introduced species is time within their grounds and in natural areas. Agenda for Botanic Gardens in consuming and expensive but can be Conservation . While Quentin Groom and successful, as described by Christoph Sharing information and resources is co-authors describe some examples of Kueffer for island ecosystems. Removal crucial for solving major environmental negative introductions from botanic of invasive species is crucial for the problems. The paper by Andrea Kramer gardens, Olivier Filippi and James conservation of threatened plants and and Abby Hird describes how BGCI is Aaronson make the point that not all more broadly for ecological restoration. developing its databases to help share exotic plants introduced for use in In March this year a group of leading information on invasive species gardens and amenity planting are bad. botanic gardens met with BGCI to plan management between botanic gardens the first steps towards a global and how collaboration can be further BGCI is currently preparing an online Ecological Restoration Initiative. You can strengthened. The paper by Peter Symes Toolkit to support implementation of the read more about this on BGCI’s website. describes practical examples of GSPC. We will include the codes of BGCI has agreed to coordinate this collaboration between botanic gardens conduct on invasive species along with initiative as it develops. Botanic gardens and plant health agencies in dealing with other guidelines and practical case have so much to contribute to restoring invasive plant pests and diseases. studies in the section on Target 10: the damaged earth – tackling invasive Voluntary codes of conduct, such as Effective management plans in place to species is an important part of the those described by Sarah Reichard and prevent new biological invasions and to action. Vernon Heywood can remind botanic manage important areas for plant gardens of the steps they should take in diversity that are invaded . We will be relation to invasive plants and of their pleased to inform you when the Toolkit is own responsibilities to ensure that plants available for review and welcome input in living collections do not contribute to from you to make this a successful the problem. Guidelines and examples resource for plant conservation around Sara Oldfield of ‘best practice’ in relation to invasive the world. Secretary General, BGCI

02 BGCI • 2011 • BGjournal • Vol 8 (2) • 02 Authors: Andrea Kramer and Abby Hird

BUILDING AN INTERNATIONAL SENTINEL PLANT NETWORK

Botanic gardens should be expanding their leadership Specifically, it has been proposed that botanic gardens and arboreta from around role in addressing invasive species and a Sentinel Plant the world work together to form an ISPN, where living plant collections information Network could facilitate this is dynamically connected and capable of serving as an early warning system to predict, detect, and prevent the incursion of new invasive pests (insects, plant Introduction Plant Network; and describe the steps pathogens, or invasive plants). The idea that BGCI and the botanic garden of a sentinel network focused on invasive nvasive plants, pests and pathogens community can take to move the idea of species is not new, and in a few cases are among the greatest threats to the an International Sentinel Plant Network model programs (such as ’s Iworld’s biodiversity and they pose a (ISPN) from a concept to a reality. expatriate plant pilot program) have been significant threat to global economic successfully implemented on a national health (Pimentel et al ., 2005), with An International Sentinel Plant scale (see Britton et al ., 2010 and Box 1). estimated costs of US$350 billion Network annually (Sheppard et al ., 2003). Botanic A clear example of why an ISPN could gardens play an important leadership It is estimated that 30-40% of known help mitigate environmental and role in protecting the world’s plant plant species are grown in living economic costs via early detection and diversity and minimizing the impact of collections of the more than 2,500 prevention of new pests comes from the invasive species. Many botanic gardens botanic gardens and arboreta 2002 discovery of the Emerald Ash Borer and arboreta work individually and throughout the world. Often, species are in Michigan, United States. The collaboratively to address invasive maintained at gardens not in the country infestation of this beetle (native to Asia) species issues by: 1) educating visitors or even on the continent in which they was not identified in time to eradicate it about invasive plant, pathogen, and are native. This presents a significant and prevent its spread, and its range is insect species; 2) monitoring collections opportunity to understand and predict now rapidly increasing throughout the to evaluate the invasive potential of when and where species may become United States and Canada. After only introduced plant species in new climates invasive pests, or when and where they five years, over 53 million native ash and sharing information with relevant may be susceptible to other pests (e.g. trees ( Fraxinus spp.) were killed by the stakeholders; 3) monitoring collections fungus and insects). beetle, and in the next ten years the to identity potentially new invasive pests infestation is predicted to cost an or pathogens; 4) working with relevant estimated $10.7 billion to treat, remove, stakeholders to contain, control, and An International Sentinel and replace the more than 17 million raise awareness about invasive species; planted ash trees likely to be killed in and 5) helping public and private P“lant Network has been urban areas alone (Kovacs et al ., 2010). partners identify alternative non-invasive proposed as a formal structure In hindsight, if an ISPN had been in plant species. Given the scope and place, botanic gardens in Asia growing acceleration of invasive species under which gardens can act North American ash species potentially problems, there is a need for botanic could have reported any unusual insect gardens to continue to expand their individually and collectively to damage, and the extreme susceptibility leadership role in addressing invasive increase the predictive power of of North American ash trees to the species. Here, we describe how the Emerald Ash Borer could have been formation of an International Sentinel their collections, and to engage predicted and measures put in place to Plant Network will facilitate this; share other partners who can use this monitor and eradicate occurrences results of a worldwide survey to identify before they became too large to control. resources and expertise for a Sentinel information. ” Further, a monitoring network of gardens

BGCI • 2011 • BGjournal • Vol 8 (2) • 03-06 03 Figure 1: Map of 146 institutions responding to the ISPN survey. Colors indicate whether institutions offer assistance with pest, pathogen or plant identification to visitors (yes = green, no = orange, gray = don’t know). Ninety percent (90%) of responding institutions provide assistance on these topics. and garden visitors in the United States This survey was available in English, minimize the risks posed by insect pests, may have helped detect the pest early Chinese, and Russian, was open for three plant pathogens, or potentially new enough to eradicate it. months, and was advertised through invasive plants. An additional 29% don’t email, list serves, and other websites and yet have invasive species policies or Below, we present results of a recent newsletters. In total, 204 respondents programs in place, but would like to. global survey aimed at identifying current from 146 botanical institutions in 15 capacity to monitor for potentially new countries completed the survey (Figure 1). Monitoring and invasive insects, plant pathogens, Results revealed a solid foundation of Nearly 96% of responding institutions and plants in the botanical community, expertise, resources, partnerships and monitor collections ‘regularly’ or ‘whenever and discuss key steps botanic gardens practices already in place to understand possible’ for insect pests, while nearly and arboreta around the world can take and address invasive species problems at 89% monitor for plant pathogens and 88% to be a part of establishing an ISPN. individual institutions, but a need for more monitor for invasive plants (Table 1). formal or regular training and enhanced BGCI’s International Sentinel communication and coordination among Staff and Resources Plant Network Survey institutions in order to increase the power Some 57% of respondent institutions and impact of the network. provide their staff with regular training Support from the U.S. Department of about pests, pathogens and/or potentially Agriculture allowed BGCI to develop and Survey Results new invasive plants. An additional 37% carry out an electronic survey during the don’t yet, but would like to. Many spring of 2011 to learn more about the Policies and Programs respondents said they had adequate staff relevant expertise and policies in place Sixty five percent (65%) of responding and resources to identify insect pests at botanical institutions around the world institutions have invasive species (85.0%), plant pathogens (70.0%), and that could help form the basis of an ISPN. policies or programs in place to help invasive plants (87.3%), but many could use more, particularly to identify plant pathogens (Table 2). How often does institution Insect Plant Invasive monitor collections for: pests Pathogens Plants Many respondent institutions employ expertise to identify and address invasive Regularly 62.80% 45.10% 51.80% species, including in the fields of Whenever possible 32.80% 43.60% 36.70% horticulture (86.8%), plant Never, but this is a future priority 0.00% 2.30% 6.50% (74.3%), entomology (35.4%), plant Never 2.90% 7.50% 2.90% pathology (29.2%), and mycology I don’t know 1.50% 1.50% 2.20% (16.7%) (Figure 2).

Table 1

04 BGCI • 2011 • BGjournal • Vol 8 (2) Outside Resources and Partners Does institution have adequate Insect Plant Invasive Most respondent institutions also utilize expertise and resources to identify: pests Pathogens Plants outside resources or partners to assist in identification of insect pests (82.5%), Yes 41.00% 24.10% 59.70% plant pathogens (82.0%), and invasive Yes, but we could use more 44.00% 45.90% 27.60% plants (59.7%). Many institutions partner No, we rely entirely on partners 12.70% 21.80% 9.70% with universities or government agencies No, we don’t identify these 1.50% 7.50% 5.20% for identification (Table 3); a few I don’t know 0.70% 0.80% 0.70% institutions utilize volunteers.

Information Sharing Table 2 L M Table 3 Most institutions reported sharing information on insect pests, plant Does institution utilize outside Insect Plant Invasive pathogens, and invasive plants found in resources or partners to help identify: pests Pathogens Plants their living collections with others at least sometimes, while several institutions Yes 82.50% 82.00% 59.70% don’t currently share this information, No, but we want to 8.80% 11.30% 11.90% but would like to do so in the future No, we don’t see a need for this 6.60% 6.00% 27.60% (Figure 3). I don’t know 2.20% 2.30% 3.70% How your institution can get Partner Type Insect Plant Invasive involved pests Pathogens Plants Locally University researchers/staff/facilities 68.80% 66.00% 53.50% Be aware that identification of insect Government agency staff/facilities 41.00% 35.40% 27.80% pests, plant pathogens, and invasive Outside consultants/facilities 23.60% 21.50% 16.00% plants is an important and often limiting Volunteers 11.10% 6.90% 9.00% resource in invasive species work. Identify partners with complementary needs and resources and find ways to work together to address current invasive species problems in your Percentage of survey respondents that maintain expertise community while predicting and and resources in ISPN-related subjects preventing future invasive species. 100 %

75 % Use your living collections to support research on invasive species if you have 50 % the resources to do so. If not, make your collections available to support the 25 % research of other collaborators and partners. 0% Entomology Horticulture Mycology Plant Plant Regionally and Nationally Pathology Taxonomy Become involved in current invasive species programs or consider starting a Figure 2 L M Figure 3 program with partners. Introduce yourself to your state/provincial agencies Does your institution share information with others? involved with invasive species monitoring and prevention, and communicate regularly with them on any suspicious insect, pathogen, or plant detected in your living collection.

Globally Update your institution’s collections information in PlantSearch to facilitate Share information on a regular basis communication, collaboration and Sometimes share information research using your living collections. Don’t share information but would like to It is quick, easy, and FREE. Every living Don’t see a need to share information collection, large and small, can help Don’t know if information is shared support collections-based research and collaboration for threatened as well as

BGCI • 2011 • BGjournal • Vol 8 (2) 05 BOX 1: Examples of what botanic gardens and networks are doing to address invasive species Acknowledgements Insect pests and plant Invasive plants pathogens Thanks to all survey respondents, and to • The European Botanic Gardens Suzanne Sharrock, Xiangying Wen, Igor • With support from the US Consortium shares information and Smirnov, Nikita Mergelov, Mikhail Department of Agriculture, the policy on potentially invasive alien Romanov, Ekaterina Eglis, and Brigitta American Public Gardens Association plants in botanic gardens: Wimmer for assistance with survey is working with the National Plant http://plantnetwork.org/ebg- distribution and translation in Europe, Diagnostic Network to engage public consortium/alien-plants/ , China and Russia. garden professionals, volunteers, and visitors in the detection and diagnosis • The Chicago Botanic Garden has References of high consequence pests and endorsed the Voluntary Codes of pathogens: www.publicgardens.org/ Conduct for Botanic Gardens and is , Britton, K. O., P. White, A. Kramer, and content/sentinel-plant-network. implementing the Codes as detailed G. Hudler. 2010. A new approach to in its invasive plants policy: stopping the spread of invasive insects • The Morton Arboretum’s online Plant www.chicagobotanic.org/research/ and pathogens: early detection and Health Care Reports provide detailed conservation/invasive/policy.php. rapid response via a global network of monthly updates on the occurrence sentinel plantings . New Zealand Journal of pests and pathogens on their • The Australian Botanic Gardens Weed of Forestry Science 40 : 109-114. collections and in the Chicago area: Network was established in 2003 and www.mortonarb.org/tree-plant- includes 75 member institutions that , Kovacs, K. F., R. G. Haight, D. G. advice/category/97/plant-health-care developed common invasive plant McCullough, R. J. Mercader, N. W. -reports.html. policies and procedures, as well as a Siegert, and A. M. Liebhold. 2010. Cost weed risk assessment procedure and of potential emerald ash borer damage • The Royal Botanic Gardens management software (Spencer et al ., in U.S. communities, 2009-2019 . Melbourne has developed a Pest 2006): www.bganz.org.au/resources. Ecological Economics 69 : 569-578. Database, Biosecurity Policy, and Weed Strategic Plan to provide • In the U.S., staff at the University of , Pimentel, D., R. Zuniga, and principles and practices that Washington Botanic Garden and D. Morrison. 2005. Update on the reduce the risk of new pest Montgomery Botanical Center have environmental and economic costs introductions to and from its partnered with others to develop a associated with alien-invasive species in landscape: www.rbg.vic.gov.au/ Weed Risk Assessment for botanic the United States . Ecological horticulture/environmental- garden decision making: Economics 52 : 273-288. management/biosecurity and p. 7-13 www.bgci.org/files/Dublin2010/ in this issue. papers/Husby-Chad.pdf. , Sheppard, A. W., R. Hill, D.-F. R.A., A. McClay, T. Olckers, Q. Jr.P.C., and H. G. Zimmermann. 2003. A global review of risk-benefit-cost analysis for invasive species by uploading a simple access information about specific the introduction of classical biological spreadsheet of taxa maintained in living resources, expertise, and eventually control agents against weeds: a crisis in collections to BGCI’S PlantSearch plant collections at gardens around the the market? Biocontrol News and database. Additional instructions can be world. This information will help form Information 24 . found here: www.bgci.org/usa/plant the basis of an International Sentinel searchinstructions. Plant Network, and allow us to deliver , Spencer, R. D., C. Preston, J. H. Watts, tools, information and updates to and N. D. Crossman. 2006. Managing Use PlantSearch now to connect directly appropriate staff at botanical institutions. weeds in Australian botanical gardens . to other living collections managers on a Proceedings of the 15th Australian species-by-species basis. For example, Conclusion Weeds Conference, eds C. Preston, use PlantSearch’s request function to JH Watts and ND Crossman: 679-682. ask other garden staff if they have There is a great need for action to detected certain pests on a specific prevent the economic and environmental Andrea Kramer plant, or if they have seen invasive impacts of future insect pests, plant BGCI US at Chicago Botanic characteristics in certain plant species in pathogens, and invasive plants, and Garden certain environments. botanic gardens around the world have 1000 Lake Cook Road the resources and expertise to help. An Glencoe, Finally, make sure your institution’s International Sentinel Plant Network can IL 60022, GardenSearch profile is up-to-date make this work more coordinated and USA (www.bgci.org/garden_search.php), impactful by supporting and expanding especially if you maintain resources, current efforts to monitor and connect Abby Hird expertise, and policies relevant to an collections, share information, and BGCI US at the Arnold ISPN (see Figure 2). Future updates to collaborate at local, regional and global Arboretum of Harvard University BGCI’s databases will allow users to levels.

06 BGCI • 2011 • BGjournal • Vol 8 (2) RBG Melbourne staff removing Eryngium agavifolium - a species noted for eradication from the Gardens due to observation of heavy recruitment in aquatic marginal environments (RBG Melbourne)

BIOSECURITY ROYAL BOTANIC GARDENS MELBOURNE

Author: Peter Symes

Increasing globalisation means that botanic gardens 2009). For example, seeds are often purchased over the internet and readily must set a priority agenda to develop biosecurity posted to a customer anywhere in the world, and these packages are not management, policy and practices to reduce the risk always intercepted by quarantine services. An international traveller with of introducing or spreading invasive species. seed or pest-contaminated footwear could easily visit a botanic garden on their first excursion, and walk onto a garden Introduction bed to take a photograph. It is likely that every botanic garden iosecurity describes the protection around the world will have serious exotic Over the last decade, a greater emphasis of living plant assets, pests to consider as threats to living has been placed on the protection of Benvironmental habitat, and plant collections. These risks should also horticultural industries from pest industries from biological threats such as be considered in the context of climate incursions in Australia with Biosecurity ‘pests’ that may cause damage or change that has the potential to create Plans developed by Plant Health Australia disease. The term pest is accepted as a conditions suitable for new and in association with many agricultural generic definition (IPCC, 2011) for a emerging exotic pests. Furthermore, industries and the Nursery and Garden biological threat that is detrimental to globalisation has increased the fluidity of Industry (PHA, 2008). For southern biodiversity, natural habitats, and plant world-wide transport systems, and Australian botanic gardens, future serious health. Some examples include subsequently, the chances of a serious exotic pests include Asian Gypsy Moth, pathogenic micro-organisms, insects, pest finding purchase in another country, Dutch Elm Disease ( Ulmus spp.), mites, pest animals, and pest plants. region or garden (Victorian Government, Eucalyptus/Guava Rust (see Box 1),

BGCI • 2011 • BGjournal • Vol 8 (2) • 07-13 07 Box 1: Eucalyptus/Guava Rust

In April 2010, Myrtle Rust (MR) Uredo 100 km from the Victorian border. and control is also a huge challenge as rangelii , a member of the Infections have already occurred in this mostly relies on frequent ‘eucalyptus/guava rust complex’ was botanic gardens in NSW. As MR is applications of full coverage chemical detected for the first time in NSW, severely infecting plants in natural areas sprays which are unsustainable from Australia. Myrtle Rust has been found as well as garden situations, it may lead an environmental and resource infecting a wide range of both native to some species (which have not perspective. and exotic plants belonging to the developed natural resistance against the Myrtaceae family, including the disease) becoming threatened. The In March 2011, the Australian National familiar Eucalyptus spp., Melaleuca reduction or loss of plant species would Botanic Gardens convened a National spp. and Leptospermum spp. also likely impact the natural ecology Myrtle Rust Workshop to consider the Myrtaceae is an iconic plant family in and life cycles of other organisms. threats from Myrtle Rust to Myrtaceae Australia with many endemic species. in natural habitats, and in ex situ plant The disease has spread rapidly along RBG Melbourne has implemented collections. More information can be the eastern seaboard of Australia and precautionary procedures and found at the Council of Heads of is now found from Northern surveillance programs. However, rust Australian Botanic Gardens website. Queensland to Southern NSW in fungi are easily spread by spores via the http://www.anbg.gov.au/chabg/myrtle- bushland, gardens and nurseries, wind, on people’s clothing or on rust/index.html (State of New South Wales, 2011) with vehicles, and it will be difficult (if not some detections occurring only about impossible) to eradicate. Containment CHABG, 2011.

Pine Pitch Canker and Sudden Oak Fireblight is a devastating disease introduced into RBG Melbourne’s living Death. These threats highlight the need particularly for the pome fruit industry plant collections. Early in 2003, to be prepared for potentially (mainly apples and pears) and had very horticultural coordinators at the Garden devastating pest incursions. significant implications for international initiated a management project to trade. The subsequent eradication develop a Weed Risk Assessment At the Royal Botanic Gardens Melbourne program that removed the few infected Process (WRAP). A working group was (RBG Melbourne), the high plant plants, and a large number of potential subsequently formed comprising both diversity of about 10,000 species means host species also resulted in the loss of horticultural and botanical staff to assist that there are a great number of plants wild-collected plants from Rosaceae with further development of the WRAP, suitable for hosting serious exotic pests, with irreplaceable plants from Southern and to develop a Weed Strategic Plan. especially when combined with close China. Also removed were important RBG Melbourne also worked closely proximity to trade and travel pathways landscape specimens including with staff from the Department of into Victoria. magnificent trees of Pyrus pashia which Primary Industries Victoria (DPI Victoria) had been growing in RBG Melbourne for to improve the risk assessment Currently, biosecurity is included as a decades. Whilst the eradication program components. Strong interest in the matter for attention within the RBG was successful, the importance of active process and valuable observations of Melbourne Risk Management Plan. Pest monitoring and surveillance was plant invasiveness by horticultural staff incursions that result in significant highlighted and has resulted in also helped refine the WRAP. In 2004, damage to the living collections are heightened awareness, planning and the Nursery Coordinator developed an ranked as a high strategic risk to the precautionary measures in dealing with interim WRAP database to improve the organisation. While RBG Melbourne has biosecurity matters within RBG processing and recording of weed risk a responsibility to protect its living Melbourne during the past decade. In assets, it also recognises the magnitude the interim, hygiene and sanitation of inadvertently spreading pests beyond practices were implemented and a its managed land that could damage hygiene protocol document was natural biodiversity and plant-based developed to limit the risk of another industries. undetected incident such as this occurring again or if it was to happen Background that there would be improved containment measures in place. Early warning – Fireblight strikes! In 1997, the RBG Melbourne had the Invasive plants management unenviable position of Fireblight ( Erwinia Prior to 2003, botanical staff had amylovora ) being found on some assessed the invasive potential of plants Cotoneaster spp. (Rosaceae) by a proposed for sale by the Growing visiting scientist (Jock et al ., 2000). This Friends. However, there was no formal was the first record of this serious exotic risk assessment or substantive process Front screen of the WRAP software pathogen being found in Australia. to address the weed risk of plants being package

08 BGCI • 2011 • BGjournal • Vol 8 (2) ‘Asparagus’ Phytophthora symptoms on Agave attenuata (RBG Melbourne)

organism originally recorded in 1995 damaging culinary asparagus plants being grown over 40 kilometres to the east of the Gardens in Cranbourne (Cunnington et al ., 2005). It is possible that the pest originally entered RBG Melbourne via soil supplies as Cranbourne is a common source for sandy loams used in landscapes all over Melbourne. RBG Melbourne had held fears that this disease may also infect Australian plants within natural habitats that had been classified within Agavaceae such as Doryanthes palmeri or D. excelsa . However, these plants appear to not be susceptible.

In October 2010, Phytophthora aff. megasperma was detected damaging Bulbine vagans – not a member of Agavaceae, but related in order through assessment. An information resource of the WRAP by the Australian Nursery Asparagales. Bulbine vagans is native to ‘Garden plants as environmental and and Garden Industry and to devise a northern NSW and Queensland, agricultural weeds, resource and programme for assessing 1,000 common Australia. This raises the biosecurity information pack ’ was developed by ornamental plants available in the issue of the risks for the diseases to botanical staff for botanic gardens and industry using the WRAP. A researcher spread to natural habitats of B. vagans . public education and made available as has been employed by the industry and a download from the RBG Melbourne the result of the assessment should be To consider further, what would be the website (RBG Melbourne, 2011a). known in about a year’s time. (See also implications of a successful incursion of RIRDC, 2011). this pathogen into natural habitats of Later in 2004, the then Weeds Agave spp. in Southwest USA? Cooperative Research Centre (Aust.) The WRAP project that was initially provided funding for an Australian derived at RBG Melbourne to reduce the Diplodia on Pines Botanic Gardens Weeds Network risks of introducing or spreading invasive In June 2010, unusual symptoms of (ABGWN) workshop which was held in plants has now developed into a national dieback on Pinus muricata were Melbourne and led by RBG Melbourne initiative, receiving funding and being submitted to Crop Health Services, DPI botanical staff to confirm policy and the accepted by weed scientists and Victoria. Symptoms identified included WRAP for adoption across Australia. In horticultural industries alike. stem cankers and dieback, needles 2005, the Council of Heads of Australian dying and resin flow from affected Botanic Gardens (CHABG) endorsed a Pest Incursions - Case Studies branches. The initial diagnosis was common Weed Policy for Australian reported as Botryosphaeria spp. This botanic gardens, and this was followed ‘Asparagus’ Phytophthora ‘weakly’ pathogenic pest is a common by the development of a federally funded In September 2000, an undescribed secondary disease in stressed plants and customised software version of the Phytophthora aff. megasperma and was relatively frequent around the WRAP which is a free download (Asparagus Phytophthora) was detected RBG Melbourne due to over a decade of available from the Botanic Gardens on Agavaceae in RBG Melbourne for the unprecedented drought. However, the Australia and New Zealand (BGANZ) first time in Australia, and possibly the RBG Melbourne sought further website (BGANZ, 2011). world. Within two months, about 70 identification to species level. Further plants from Agavaceae (particularly DNA sequence data established the A scientific analysis of the WRAP was Agave spp.) were killed and or removed identity of the pathogen as Diplodia published in the journal Plant Protection due to severe infection. This disease africana and this was also later detected Quarterly. The paper assessed the has been a continuing and significant from a nearby Pinus patula. D. africana discriminatory power and potential cut- problem to date with devastating was first described as a new species in off scores for the test (Virtue et al ., 2008). impacts primarily on plants from South Africa, where it was isolated from The potential for application of the Agavaceae. Over ten irreplaceable, wild- shoots of Prunus spp. However, this WRAP to industry was noted in the collected Agave spp. were killed outright incursion on Pinus spp. in the RBG paper and, in April 2011, an industry by this disease. Interestingly, in 2005, Melbourne appears to be the first record workshop was held at the Royal Botanic this Phytophthora spp. was finally described anywhere in the world. Gardens Sydney to discuss the adoption confirmed via DNA analysis as the same Similarly to other Diplodia infections,

BGCI • 2011 • BGjournal • Vol 8 (2) 09 Blue staining of timber symptomatic of Diplodia spp. infections (RBG Melbourne) Diplodia africana on Pinus muricata (RBG Melbourne) it was thought that predisposing biotic or Melbourne. From September 2010, disease as soon as possible under abiotic stresses were required to initiate further surveillance by Biosecurity suitable conditions to reduce risk of infection. In this case symptoms seemed Victoria did not detect D. africana in any spreading fungal spores (low wind to be related to previous significant hail Pinus spp. within or outside RBG speed, dry weather), even though damage that occurred to trees in March Melbourne. Due to the possible risk to pathogenicity had not yet been fully 2010. The area was barricaded and a commercial pine plantations and amenity determined. In October 2010, the two ban imposed on movement of Pinus trees in general, it was decided to infected trees were removed as a joint material within and out of RBG remove these trees to contain the operation between Biosecurity Victoria

Table 1 - Selected new pest incursions to RBG Melbourne

Detection Date Pest Detected Hosts Comments

May 1997 Fireblight Erwinia amylovora Cotoneaster and Sorbus. Significant loss of unique provenance and landscape specimens. Disease eradicated.

Sep 2000 ‘Asparagus Phytopthora’ Mainly Agavaceae Significant loss of unique wild-collected material and Phytophthora aff. megasperma landscape specimens. Limited control achieved by applying phosphonate fungicides.

Jan 2004 Fusarium Wilt (Palms) Fusarium Phoenix canariensi s One infected palm removed under quarantined oxysporum f . sp. canariensis conditions. No further infections detected to date

Jul 2004 Phytophthora niederhauseria Xanthorrhoea australis First record in Victoria. Plant removed. No further detections. Has since been found as records elsewhere in Victoria from taxonomic reviews.

Nov 2004 Mahonia Rust Mahonia fortunei First known record in Victoria on Mahonia spp. (Cumminsiella mirabilissima )

Jun 2010 Diploda africana Pinus muricata and First known record in the world infecting Pinus spp. Pinus patula Trees were removed under quarantined conditions. Pinus muricata was an only accession for RBG Melbourne.

Oct 2010 ‘Helleborus Black Death’ Helleborus orientalis ; First known record in Australia, since been found in [Helleborus Net Necrosis Virus H X sternii gardens to the east of Melbourne including (HeNNV)] symptomless plants. Research continuing with Biosecurity Victoria.

10 BGCI • 2011 • BGjournal • Vol 8 (2) and RBG Melbourne staff under quarantined conditions. Subsequent pathogencity testing of D. africana completed in December 2010 ultimately found it to be less severe than the more common D. pinea . If further incursions of D. africana occur this is now considered to be a local management responsibility for RBG Melbourne.

This incident highlights the importance of avoiding assumptions about disease symptoms and or being satisfied with identifications to genus level (which is often influenced by testing costs). If the scenario had involved a more serious pathogen, and RBG Melbourne had not requested further identification, it is conceivable that an epidemic on Pinus spp. may have ensued, damaged commercial interests and opened RBG Melbourne to scrutiny and loss of reputation in the community.

These case studies and new incursions Completion of Diplodia africana eradication operation -disinfection processes underway (D. Smith0 highlight the importance of biosecurity to protect botanical living assets, natural Relationships with Plant Health very responsive to notifications of habitats and industries. The value of Agencies unusual pest symptoms. Personnel will botanic gardens living plant collections often make the effort to visit and take and expert staff is emphasised in RBG Melbourne has fostered highly specimens for analysis at no cost. In supporting the work of plant health collaborative relationships with plant 2006, Plant Standards undertook a agencies for detecting pest incursions health agencies both within and outside Hazard Site Surveillance program that early. Active surveillance, accurate Australia. In particular, Plant Standards, operated for two years to inspect large identification, containment, and Biosecurity Victoria has recognised the gardens and urban landscapes for establishing pest pathogenicity and host sentinel value of the diversity of RBG serious exotic pests which included RBG range are vital lessons that were learnt. Melbourne’s plant collections and are Melbourne due to its proximity to the city. There have also been other collaborative projects with Biosecurity Australia in screening for particular exotic pests. Being able to provide current plant records and/or horticultural staff assistance to locate host plants improves the efficiency of the site surveillance, and is noted and welcomed by the personnel involved.

In 2007, RBG Melbourne began assisting with the New Zealand (NZ) Expat Plants Project (Biosecurity New Zealand, 2011) which was a component of the Better Border Biosecurity (B3) program. The intent of this forward thinking project was to identify NZ plant collections growing overseas that could then be used as international sentinels of emerging pests that may threaten NZ flora. Some pest affected specimens from RBG Melbourne were collected by NZ researchers under phytosanitary conditions to consider for pest risk to NZ’s natural resources. Communication Removal of Pinus patula infected by Diplodia Africana (D. Smith) has continued with the B3 program

BGCI • 2011 • BGjournal • Vol 8 (2) 11 International Course in Botanic Garden Management (BGCI)

Professional and Public and also its responsibility to prevent pest Education threats to others. The organisation has Symptoms of Helleborus Black Death (HeNNV) on adopted the philosophy that effective Helleborus x hybridus (RBG Melbourne) In March 2010, BGCI and BGANZ biosecurity includes the implementation delivered the International Certificate in of both border quarantine and internal when pests on NZ flora are identified. It Botanic Gardens Management course in pest management practices such as is also understood that other BGANZ Singapore (BGCI, 2011) to a range of Integrated Pest Management (IPM) (see member Australian botanic gardens have participants generally from SE Asia. Two Figure 1). assisted with this project. of the modules under horticulture led by RBG Melbourne addressed biosecurity Principles Pest Database through management of invasive plants Underpinning the RBG Melbourne and pests. Biosecurity Policy are eight principles: In 2006, conceptual planning began for 1. Seek to prevent pest excursion, developing a system that would A range of training is regularly delivered by incursion and further spread. integrate recording, education and horticultural staff and external experts for 2. Manage risk of transport of landscape management of pest problems in RBG employees, friends and volunteers. materials across management Melbourne. In 2008, a pest database Information relating to biosecurity and boundaries. was completed as a component of the pest management has also been provided 3. Conduct regular surveillance. RBG Melbourne’s living plant collections via the website (RBG Melbourne, 2011b). 4. Promote plant health according to the database. It is now possible to produce prevailing environmental and climatic comprehensive reports of particular Policy and Procedures conditions, and available resources. hosts, known distribution, treatment 5. Implement effective hygiene and history, images of symptoms, etc. This In 2010, RBG Melbourne improved its sanitation practices. has become a valuable management biosecurity strategy in completing an 6. Conduct regular employee training tool toward improving pest management organisational Biosecurity Policy and is and visitor education programs. within RBG Melbourne. Being linked to currently reviewing the associated 7. Maintain and develop effective the plant collections database also procedures. Within the policy, RBG relationships with plant health agencies. means that changes in plant Melbourne acknowledges the importance 8. Continue to develop and improve nomenclature or location names are also of the stewardship of its living assets to procedures for effective monitoring, readily updated. protect them from exotic pest threats, recording and managing pests.

Pest module from the Living Plant Collections Database

12 BGCI • 2011 • BGjournal • Vol 8 (2) , Jock S., Rodoni B., Gillings M., Kim W.S., Copes C., Merriman P. and Sources of Plant and Landscape Materials Geider K. 2000. Screening of t r

o ornamental plants from the Botanic p

s Gardens of Melbourne and Adelaide n a r for the occurrence of Erwinia T

‘Border Quarantine’ t Botanic Garden s amylovora. Australasian Plant

Practices e Border P Pathology 29 , 120–128. l a i

t , (PHA). 2008. Plant Health Australia. n e

t National Nursery and Garden Industry o

Potential pathways P Biosecurity Plan , Version 2 , (Plant and impacts on Health Australia, Canberra, ACT). other stakeholders http://www.planthealthaustralia.com.a RBG MELBOURNE Managed Land u/index.cfm?objectid=56547079- D8A5-9C78-C2E3FB24155327BC. Host , (RBG Melbourne). 2011a. Royal Botanic Gardens Melbourne. http://www.rbg.vic.gov.au/horticulture/ environmental- Integrated Pest management/biosecurity (Accessed Management 2011). (Expression) Disease Damage , (RBG Melbourne). 2011b. Royal Botanic Gardens Melbourne. http://www.rbg.vic.gov.au/horticulture/ Pest Environment environmental- Pest Triangle management/biosecurity/pest-manage ment (Accessed 2011). Figure 1- Border Quarantine and Pest Triangle Schematic , (RIRDC). 2011. Rural Industries Pest Triangle adapted from (Agrios, 1988) Research and Development Corporation Conclusion References http://www.rirdc.gov.au/programs/nati onal-rural-issues/weeds/weeds—- There is an increasingly vital role for , Agrios, G.N. 1988. Plant Pathology, phase-2-research-projects/weeds—-p botanic gardens to fulfil in protecting the 3rd edition . Academic Press, Inc: hase-2-research-projects_home.cfm biosecurity of natural environments, California. (Accessed June 2011). cultural landscapes and industries. , Biosecurity New Zealand. 2011. , State of New South Wales 2011. Whilst the high plant diversity intrinsic to http://www.biosecurity.govt.nz/publica Department of Primary Industries, botanic gardens may be seen as a risk tions/biosecurity-magazine/issue- Biosecurity, Myrtle Rust Website to biosecurity, it can actually provide an 82/expat-plant-comm (Accessed May http://www.dpi.nsw.gov.au/biosecurity ‘early warning’ mechansim through 2011). /plant/myrtle-rust (Accessed June sentinel plants to herald the incursion of , (BGANZ). 2011. Botanic Gardens of 2011). a new invasive species. This early Australia and New Zealand. , Victorian Government .2009. identification of pests provides greater http://www.bganz.org.au/resources Biosecurity Strategy for Victoria opportunity for the success of (Accessed May 2011). (DPI, Biosecurity Victoria, May 2009). containment and eradiction programs. , (BGCI). 2011. Botanic Gardens , Virtue, J.G., Spencer, R.D., Weiss, World-wide, botanic gardens can readily Conservation International. J.E. & Reichard, S.E. 2008. Australia’s share their expertise and observations http://www.bgci.org/resources/event/0 Botanic Gardens weed risk from practitioner to scientist, to work 222/) (Accessed May 2011). assessment procedure . Plant with plant health agencies and produce , (CHABG). 2011. Council of Heads of Protection Quarterly 23 (4): 166–178. a more robust surveillance network. Australian Botanic Gardens. Increasing globalisation also means that http://www.anbg.gov.au/chabg/myrtle- Peter Symes botanic gardens must set a priority rust/index.html (accessed June 2011). Curator, Environmental Horticulture agenda to develop biosecurity , Cunnington J.H., de Alwis S., Pascoe Royal Botanic Gardens Melbourne management, policy and practices to I.G., Symes P. 2005. The ‘asparagus’ (Private Bag 2000) reduce the risk of introducing or Phytophthora infecting members of Birdwood Avenue spreading invasive species. Botanic the Agavaceae at the Royal Botanic South Yarra gardens have readily demonstrated Gardens , Melbourne. Australasian Australia 3141 leadership through dedicated personnel Plant Pathology 34 , 413–414. Tel: + 61 3 9252 2347 in reducing the risk and impacts from , (IPPC). 2011. International Plant Fax + 61 3 9252 2348 invasive species upon biodiversity. Protection Convention Email: [email protected] https://www.ippc.int/IPP/En/default.jsp (Accessed May 2011).

BGCI • 2011 • BGjournal • Vol 8 (2) 13 Author: Christoph Kueffer

PREVENTING AND MANAGING PLANT INVASIONS ON OCEANIC ISLANDS

Figure 1: On oceanic islands, high elevation heather formations are among the very few habitats not yet heavily invaded. With climate change, increased disturbance and the introduction of new non-native species this resistance may decrease and preventive measures should be a priority (Eva Schumacher)

The impacts of alien invasive species are particularly or Kueffer and Loope, 2009) and I will therefore in this article only focus on severe on islands, but efforts are underway to address selected aspects that are in my view particularly relevant for an effective this threat. prevention and management of plant invasions on oceanic islands.

If not botanic gardens, who else? Introduction is confronted with the challenges of (i) preventing further introduction of On islands, botanic gardens have a ceanic islands are infamous for the potentially invasive non-native species, particular responsibility for invasive plant extent and impacts of invasions by (ii) containing the spread of already management because they are often the Onon-native species. Globally, introduced non-native species, and (iii) only organisations with substantial hundreds of different invasive plant mitigating the impacts of established specialised botanical expertise and species have invaded island ecosystems invasive species. Comprehensive related international connections. and threaten native biodiversity, and the documents that treat these different A reliable taxonomy of established non- same is true for other groups of non- management phases specifically for native plants and a rapid identification of native organisms (e.g. Caujapé-Castells islands are readily available on the internet new introductions are the basis of et al ., 2010; Kueffer et al ., 2010a). (e.g. “ Guidelines for Invasive Species effective prevention and management of Management of invasive plants on islands Management in the Pacific ”1 plant invasions. Many botanic gardens

14 BGCI • 2011 • BGjournal • Vol 8 (2) • 14-17 1 http://www.sprep.org/att/publication/000699_RISSFinalLR.pdf on islands maintain a continuously Many non-native plants remain important difficult and costly. However, prevention updated database of the native and non- for agriculture, forestry and daily life on is very challenging too and new native flora (for a compilation of islands, and some of them have become innovative biosecurity solutions and examples of such online databases see allies of nature conservation; for instance continuous learning to improve existing Caujapé-Castells et al ., 2010, pp. 113). by stabilising soils, preventing invasions good practice approaches are needed. by other and potentially more problematic Above all, preventative measures need As key players in the horticulture sector, non-native plants or providing food to to be simple and take the limited botanic gardens should be role models native fauna (Kueffer et al ., 2010b). financial and human resources of island of good practice, and the St. Louis Managers and scientists on islands societies into consideration. Codes of Conduct 2 can serve as a increasingly recognize the beneficial role guideline. The example of the of non-native plants in heavily altered Few, if any, oceanic islands Conservatoire Botanique National de “novel ecosystems”. Sometimes the same Mascarin (CBNM) illustrates how botanic non-native plant species can play a h“ave yet implemented an gardens can take on a leadership role in beneficial role in one habitat and yet have effective biosecurity system that education, awareness building and major negative impacts in a neighbouring policy formation. The CBNM was for habitat, thus posing new challenges to is able to substantially reduce instance a leading organisation in the invasive species management. Non-native the rate of new introductions of preparation and implementation of the cinnamon ( Cinnamomum verum ) for invasive species management strategy instance is beneficial in the Seychelles for non-native organisms. of La Réunion 3. As the following biodiversity management in mid-elevation ” paragraphs highlight, the involvement of forests (Kueffer et al ., 2010b) but is a botanic gardens in invasive species major problematic invader of nearby Increased travel and transport mean that management can include a broad range montane cloud forests. introduction rates of new organisms to of activities such as the promotion of the islands have become so high that use of native plants, ex situ propagation Prevention – pragmatic effective control at borders is almost of native plants, restoration of invaded solutions and innovations are impossible. Daily, non-native organisms habitat, networking actors, and outreach needed are transported to islands around the to the general public. world and inevitably some of these It is generally believed that the species will not be detected at borders. Botanic gardens have the prevention of new introductions of How prevention can work in an potentially invasive non-native increasingly globalised world is not n“ecessary expertise and organisms is more effective than the evident. A solution may lie in developing networks to be key players in later management of problematic multi-layered biosecurity systems based invasions. Indeed, eradication or on shared responsibilities among many controlling invasive species. containment of a spreading non-native agencies and citizens, with post- ” species and the management of introduction detection as a second established invasive species is very important filter after border control. Although plant protection is not the focus of this article, it is also important that botanic gardens act responsibly with respect to the prevention of new introductions of plant diseases and pests, which can spread rapidly across small islands and affect the majority of the individuals of a vulnerable native plant species in a short period of time (Caujapé-Castells et al ., 2010).

Most non-native plants are friends not foe, and sometimes they are both at once

While some non-native plants are indeed an important threat to island biodiversity, most of them are not problematic. In fact, the presence and abundance of many non-native plants on islands are due to past anthropogenic habitat destruction or the result of deliberate planting for forestry, restoration of degraded land or landscaping, rather than an active Figure 2: The native plant ex situ collection at Barbarons Biodiversity Center on Mahé, Republic of Seychelles invasion of undisturbed natural areas. (Eva Schumacher)

2 http://www.centerforplantconservation.org/invasives/DownloadPDF/bga.pdf BGCI • 2011 • BGjournal • Vol 8 (2) 15 3 http://www.cbnm.org/component/docman/doc_download/93-strategie-de-lutteinvasives Possible invasive non-native species was at first developed relatively Promote native and non- that pass through border control must independently of stakeholders, invasive alternative plants be detected as early as possible after especially the plant industry, and introduction while they are still localized consequently acceptance by A particular important strategy to and eradication is still feasible (Kueffer stakeholders was low. Thanks to support the prevention of new and Loope, 2009). This will require committed representatives of the plant introductions of potentially invasive non- regular systematic early detection industry a more participatory process native plants is formulated in the St. surveys as exemplified by the Hawaiian was later initiated, which significantly Louis Code of Conduct cited above as example (Kueffer and Loope, 2009) but increased the acceptance of weed risk follows: “5. Promote non-invasive depends also on the collaboration and assessments and preventative measures alternative plants or, when possible, help awareness of other agencies – e.g. those among industry partners (Kueffer and develop non-invasive alternatives involved in road maintenance, Loope, 2009). through plant selection or breeding ”. landscaping, forestry and agriculture – Environmental degradation related to and the general public. In the Hawaiian archipelago it was also fire, droughts, deforestation, and erosion particularly effective to setup a separate is for instance a major environmental Partnerships with stakeholders Invasive Species Committee (ISC) on management challenge on many oceanic are of pivotal importance each of the different islands (Kueffer and islands. To combat erosion, even today Loope, 2009). These island-specific ISCs non-native Acacia species, which are An important lesson learnt is that allow preventative measures: early known invaders, are introduced to new stakeholder concerns and expertise detection, monitoring, awareness islands. To stop such deliberate should be built into invasive species building and outreach to be tailored to introductions that pose a severe invasion prevention and management from the the specificities of the individual islands. risk, alternative ways of restoring very beginning. In Hawaii, for instance, a For instance, on a small island such as degraded sites with native or non- weed risk assessment system with the Molokai, where everyone knows invasive, non-native species have to be aim of predicting potentially invasive everyone, effective approaches are urgently developed. For the development non-native species that should be different to those required on a highly and promotion of native plants for use in prevented – the Hawaii-Pacific Weed urbanised island such as Oahu, or a restoration – as well as, for instance, in Risk Assessment system (HP-WRA 4) – large and sparsely populated island such landscaping, horticulture or forestry, as the Big Island. botanic gardens play a key role. Many botanic gardens on islands do already Prevent future invasions, don’t invest heavily in native plant ex situ fight the ghost of past invasions propagation programmes (Figure 2).

There is a tendency in invasive species Resurrection of native management to invest most resources on biodiversity after invasion can the management of those islands and happen habitats that are already heavily affected by invasions. Once a problem is Even in the case of heavily invaded experienced, money flows. But prevention island ecosystems, there is hope. is only effective if it is one step ahead. The Removal of invasive plants and most problematic future invasions will exclusion of invasive animals from likely happen in areas that are not yet conservation management areas, either badly invaded. In contrast to already through mechanical or biological control invaded areas, un-invaded ecosystems measures, can have rapid and dramatic offer open ecological niches that are not positive effects on the recovery of native yet filled and native biodiversity is not yet plants and other biodiversity. This has for impacted through earlier invasions. instance been shown for intensively Ecosystems situated in less developed, managed conservation areas in Hawaii remoter or less disturbed regions or (Kueffer and Loope, 2009) and Mauritius islands may thus require particular (Baider and Florens, 2011; Florens et al ., attention (Fig. 1). For instance, the 2010), or native regeneration after expansion of ecotourism onto new islands biological control of Miconia calvescens or into new habitats may be a reason for in Tahiti (Meyer and Fourdrigniez, 2011). concern and should be accompanied by A striking example has recently been preventative measures, increased early reported from Conservation detection survey activities and awareness Management Areas (CMA) in Mauritius building. With environmental change and (Western Indian Ocean) (Fig. 3). Ten the introductions of new types of non- years after weeding of sites formerly native plants through land use changes, infested with Psidium cattleianum , Figure 3a: Bris de fer forest Mauritius, heavily those habitats that have been resistant to juveniles of two presumed extinct, three invaded by invasive Psidium cattleianu invasions in the past may become critically endangered and four (Claudia Baider) vulnerable too. endangered native plant species were

16 BGCI • 2011 • BGjournal • Vol 8 (2) 4 www.botany.hawaii.edu/faculty/daehler/wra References

, Baider, C. and Florens, F.B.V. 2011. Control of invasive alien weeds averts imminent plant extinction . Biological Invasions, in press. doi: 10.1007/s10530-011-9980-3

, Caujapé-Castells, J. et al . 2010. Conservation of oceanic island floras: present and future global challenges . Perspectives in Plant Ecology Evolution and Systematics 12 : 107-130.

, Florens, F.B.V., Mauremootoo, J.R., Fowler, S.V., Winder, L. and Baider, C. 2010. Recovery of indigenous butterfly community following control of invasive alien plants in a tropical island’s wet forests . Biodiversity and Conservation 19 : 3835-3848.

, Kueffer, C., Daehler, C., Torres- Santana, C. W., Lavergne, C., Meyer, J-Y., Otto, R. and Silva, L. 2010a. A global comparison of plant invasions on oceanic islands . Perspectives in Plant Ecology, Evolution and Systematics 12 : 145-161.

, Kueffer, C., Schumacher, E., Dietz, H., Fleischmann, K. and Edwards, P.J. 2010b. Managing successional trajectories in alien-dominated, novel ecosystems by facilitating seedling regeneration: a case study . Biological Conservation 143 , 1792-1802.

, Kueffer, C. and Loope, L.L. 2009. Prevention, early detection and containment of invasive, non-native plants in the Hawaiian Islands: current efforts and needs . Pacific Cooperative Studies Unit Technical Report 166, University of Hawai`i at Manoa, Honolulu, USA. http://www.botany. hawaii.edu/faculty/duffy/techr/166 Figure 3b: Bris de fer today following successful weeding and rehabilitation into native species dominated forest, including vigorous re-growth of rare species (Claudia Baider) , Meyer, J.Y. and Fourdrigniez, M. 2011. Conservation benefits of biological recorded, together with vigorous invasive species from intensively control: The recovery of a threatened regeneration of many other native managed conservation areas is one such plant subsequent to the introduction of species (Baider & Florens, 2011). The emergency measure. a pathogen to contain an invasive tree same positive trend was also found for species . Biological Conservation 144 : butterfly species (Florens et al ., 2010). Acknowledgements 106-113. Island ecosystems still harbour surprisingly high levels of relict native This article has profited from discussions Christoph Kueffer biodiversity, but this is probably only due on the list-server of the Global Island Institute of Integrative Biology to a time lag effect (“extinction debt”) Plant Conservation Network (GIPCN, Plant Ecology, and much of this biodiversity may go http://www.bgci.org/ourwork/islands/). ETH Zurich, extinct without immediate active I thank Claudia Baider and Eva Switzerland management intervention. Exclusion of Schumacher for providing pictures. [email protected]

BGCI • 2011 • BGjournal • Vol 8 (2) 17 Authors: Quentin J. Groom, Anne Ronse and Ivan Hoste

THE REASONS FOR EXOTIC PLANT INVASIONS AND WHY BOTANIC GARDENS ARE PARTICULARLY VULNERABLE

The problems caused by alien invasive plants are with reference to the National Botanic Garden of Belgium (NBGB) and other related to many aspects of human activity. Botanic northern European gardens, how botanic gardens can actively contribute to each gardens, with their experience in cultivating exotic of these scenarios.

species, are central in helping to address such Migration

problems. The range of some species is only restricted by their ability to disperse. Such species will survive in new areas, but they are unable to reach such areas by natural spread (Sax and Brown, 2000). Botanic gardens are skilful at growing introduced species, yet not all these species escape cultivation. One explanation is the hypothesis of propagule pressure (Simberloff, 2009). This hypothesis suggests that a minimum rate of propagule import is required to ensure that founder populations of aliens can establish in a novel location. Below this minimum, alien species are unlikely to find suitable habitat and will have insufficient genetic diversity to survive. This acts as a barrier to potentially invasive species, favouring those species that are more frequently imported.

A minimum rate of propagule “import may be necessary for an alien to establish. corymbosa (Ivan Hoste) ” It is clearly not only botanic gardens that Introduction invasive plants, yet there are good import alien plants. Plant propagules are ecological and evolutionary reasons why imported for all sorts of reasons, otanic gardens need to be botanic gardens are particularly liable to particularly for food. Today it is no doubt constantly alert to the possibility causing new invasions. Facon et al ., the horticultural industry that imports the Bof introducing new invasive (2006) wrote a simple synthesis of the largest range of species, either species. Even gardens with a high primary reasons for biological invasions. specifically for propagation and sale, or awareness of the problem may have In their paper they reduce the causes of as stowaways. By piggybacking on the conditions that make them prone to invasions to three basic scenarios: activities of mankind, plants can easily losing control of the plants they grow. migration change, environmental change breach once insurmountable barriers to Many of mankind’s activities can result in and evolutionary change. Here we show, dispersal (see box 1).

18 BGCI • 2011 • BGjournal • Vol 8 (2) • 18-22 Box 1: Cardamine corymbosa , New Zealand Bitter-cress

Though it is unknown how it got to recorded in the rock garden at the Britain originally, Cardamine University of Ghent and the botanic corymbosa was first recognised at the garden of Leuven. At the NBGB it has Royal Botanic Garden Edinburgh. It shown up as a fleeting visitor. During a had been noticed, as a persistent garden event, in June 2008, plants weed, by the gardeners for years were discovered at 6 out of 30 stands before it was first identified as an alien, selling plants, yet fortunately it hasn’t rather than a native Cardamine spp. established in the Garden as a result. (Braithwaite, 1991). Its explosive ripe Often, it only requires a short residence The now classical tale of how Senecio fruits, its preference for plant pots, time in a garden centre for seed to squalidus spread in Britain from Oxford combined with the constant flux of disperse from one pot into University Botanic Garden along the container plants through extensive neighbouring containers or between railways in the late 19th century, usually horticultural networks in Europe create paving stones. The ease with which it does not tell that it was already “very ideal conditions for its dispersal (Hoste proliferates puts C. corymbosa in the plentiful on almost every wall in Oxford” et al ., 2008). It has since spread all company of other ill-reputed pot at the end of the 18th century (Kent, over Britain and by the early 21st contaminants such as Cardamine 1956, 1960). Furthermore, it was century had reached the Netherlands hirsuta, Sagina procumbens and Oxalis naturalized in other distant towns, well and Belgium, where it has been corniculata . (Photo: Ivan Hoste) before Oxford was connected by railway. In at least three cases it had escaped from gardens where the seed had originally been taken from Oxford as a While the removal of dispersal barriers compared to 7,000 cultivated taxa botanical novelty (Kent, 1956). One can by human activity can explain the growing outdoors in the garden, of 100 see the same influences of botanic migration of invasive species, it does not pests and diseases recorded in the gardens, novel habitats, disturbance and explain why invasive plants are often garden, only 10 occur only on alien horticultural novelty in the introduction more successful than native species. species (Groom, 2011). While enemy histories of many species (Hulme, 2011). The enemy release hypothesis suggests release is unlikely to be the sole reason that one of the reasons for the success for the success of invasive species, it It will come as no surprise that species of invasive plants is that they are seems likely that it is a contributing which escape into the neighbourhood of released from the stress of pests and factor in some cases. botanic gardens are those that thrive in diseases that occur in their native ranges the habitats of that area. Thus a garden (Keane & Crawley, 2002). One of the Environment surrounded by wall, as in the case of observations consistent with this Oxford Botanic Garden, exports S. hypothesis is that: A large number of invasive species occur squalidus that grows on walls. Likewise, in places disturbed by human activity, a forest garden is likely to export shade- invasive alien species have such as in urban environments, on loving species and a desert garden will agricultural land and by roadsides export xerophytes (Marco et al ., 2009). In “fewer pests and diseases in their (Lozon, 1997). This may, in part, be the NBGB we have found that many of invasive ranges. explained by the creation of novel the most persistent and invasive habitats. The proximity of botanic escapes are woodland plants whose ” gardens to large urban areas, full of seeds are spread by birds (Box 2; This is certainly consistent with our novel, unexploited habitats, certainly Ronse, 2011). This is inevitable, since observations at NBGB. Although there raises the risk of new invasions being nearly half of the area of the garden are only about 350 wild native species initiated by garden escapes. consists of woodland.

BGCI • 2011 • BGjournal • Vol 8 (2) 19 Box 2: Diospyros lotus

Diospyros lotus (Ebenaceae) is a tree from south-east Europe and south-western Asia that produces edible fruits called date plums, dispersed by birds. Hundreds of seedlings of this species have had to be removed and were found up to one kilometre away from cultivated trees at the NBGB, some of them growing in wooded, undisturbed areas of the Garden (Ronse 2011). Evolution Though unconscious selection will predominantly act on annual and other D. lotus is not a particularly It has been argued that a species, when short-lived species, there is also a attractive tree and will only produce liberated from the competition, filtering process in the acquisition of seed if both male and female tree environmental stress and pests and plants. Dead plants are continually are present. Therefore botanic diseases of its native habitats, can replaced until a species or variety is gardens, rather than private evolve to reallocate its resources from found that persists. In our own garden gardens, are much more likely to be protective mechanisms into traits which an accession of Oenanthe the source of escapes, at least in confer greater invasive potential (Blossey pimpinelloides , originally from Bulgaria, Northern Europe. & Notzold, 1995). While such evolution is has escaped cultivation even though O. (Photo: Paul Borremans) generally suggested to occur in wild pimpinelloides is usually considered too populations there is certainly also cold sensitive to develop persistent unconscious selection occurring in populations in Belgium (Ronse, 2011). botanic gardens (Enßlin, Sandnera & Matthiesa, 2011). It is likely that In addition, the pool of introductions to a unconscious selection for improved garden is not unbiased. Botanic gardens survival in a garden may also mean often produce a list of seeds for selection for traits that encourage exchange with other gardens, know as weediness. an index seminum . A random survey of these lists showed that several invasive Selecting individuals that species were listed, presumably because of their high rate of seed g“row well may result in selecting production (Aplin & Heywood, 2008). for weediness. All these processes combine to favour invasive species in gardens, indeed the ” result can be seen in the inventories of A recent example is the case of Poa many gardens (Box 3; Hulme, 2011). annua f. purpurea M. L. Grant (Grant, Hybridisation has been implicated in the 2003). Hand-weeding in gardens has evolution of invasive plants (Ellstrand & apparently selected for this purple-leaved Schierenbeck, 2000). Examples are form of a practically ubiquitous weed. Its Casuarina ssp. in Florida (Gaskin et al ., dark cryptic colouration makes it more 2009); Fallopia ssp. in Belgium (Tiébré et difficult to see against dark coloured soil al ., 2011); Senecio squalidus in the UK Poa annua f. purpurea (RHS/Barry Phillips) than the normal green P. annua . (Abbott et al ., 2000) and Spartina anglica

20 BGCI • 2011 • BGjournal • Vol 8 (2) Box 3: Botanic gardens are biased towards invasive species representation of invasive plants comes from plants being grown in greenhouses in temperate countries, where they are unlikely to become a South American (8) 5.7% garden escape.

Australasian (18) 1.0% The USA was analysed separately from the rest of North America, USA (151) 3.0% because many gardens from the USA follow the voluntary codes of conduct North American - USA (41) 4.3% of the St. Louis declaration on invasive plants. The smaller percentage of European (163) 2.8% invasive species in gardens in the USA might be a result of these codes. The African (12) 4.2% greater awareness and regulation of invasive species in Australia and New Asian (12) 4.1% Zealand has undoubtedly helped Australasia have the lowest value. By random chance 0.4% These values should only be taken as a guide. They are biased by the The average percentage of 455 with a list of 455 of the most invasive availability of digitised collections; by invasive plants grown at 406 botanic plant species from the ISSG’s Global the overall size of collections; by gardens, split by continent. The Invasive Species Database uncorrected synonymy and by the list number of gardens included from each (http://www.issg.org/database, 2011). of invasive species used. continent are shown in parenthesis. All but 6% of these invasive species are Nevertheless, we can conclude that Only gardens with more than 100 grown in at least one botanical garden. the collections of botanic gardens are species in the database were used biased towards invasive species. and seed banks were excluded. If one assumes a garden’s plants are However, it is encouraging that these Synonymies of species names were chosen randomly from the pool of all the results suggest that a greater corrected, but not exhaustively. species grown, then these invasive awareness of the issue is likely to plants should occur as 0.4% of reduce the problem. The BGCI’s PlantSearch database collections. However, on average, these contains almost a million records of invasive species represent 3.0% of Based on the PlantSearch and GIS plants grown at the world’s botanic collections. Though it should be Databases 2011. gardens. This database was compared mentioned that some of this over-

across Europe (Thompson, 1991). While the filtering out of feeble taxa may all important role in educating the public. horticulture was not the cause of contribute to the evolution of While significant steps have been made hybridization in all of these taxa, the invasiveness in gardens. to address the problem of invasive close proximity of closely related taxa in plants in botanic gardens, there is still gardens undoubtedly presents an Conclusion work to be done and a clearer opportunity. In the NBGB we have understanding of the mechanisms that witnessed the in situ generation of the There are many hypotheses for why we result in problem situations is important. potentially invasive hybrid Oenothera x have an alien invasive plant problem. fallax from its two parents O. biennis and However, for each hypothesis, the cause References O. glazioviana . Similarly seedlings of relates either directly or indirectly from Hyacinthoides x massartiana are the activities of humankind. We have , Abbott, R.J., James, J.K., Irwin, J.A. & increasingly found within the park, both created a small, interconnected world, Comes, H.P. 2000. Hybrid origin of the in the collections and in semi-wild areas. and botanists, horticulturists, and Oxford Ragwort , Senecio squalidus L. This is the hybrid between the native H. botanic gardens have eagerly Watsonia 23 : 123 - 138. non-scripta and introduced H. hispanica cooperated in the process. We need to which have both been cultivated in the continually assess how we can benefit , Aplin, D. & Heywood, V. 2008. Do Seed garden for more than forty years. from this, while avoiding the drawbacks. Lists have a future? Taxon 57 (3): 1-3. Botanic gardens are a small but Despite there being little research on this significant part of the invasive plant , Blossey, B. & Notzold, R. 1995. subject, it seems likely that a problem. Yet botanic gardens are also Evolution of increased competitive combination of unconscious selection, leaders in good practice for horticulture ability in invasive nonindigenous plants: hybridization between genotypes and and conservation and can play an a hypothesis . J. Ecol. 83 : 887-889.

BGCI • 2011 • BGjournal • Vol 8 (2) 21 , Braithwaite, M. 1991. New Zealand , Groom, Q.J. 2011. Gall causing , Kent, D.H. 1956. Senecio squalidus L. Bittercress , Cardamine uniflora. organisms in the National Botanic in the British Isles. 1. Early records (to B.S.B.I. News 58 : 38-39. Garden of Belgium . Scripta Botanica 1877) . Proc. Bot. Soc. Br. Isl. 2: 115– Belgica 47 : in press. 118. , Ellstrand, N.C. & Schierenbeck, K.A. 2000. Hybridization as a stimulus for , Gaskin, J.F., Wheeler, G.S., Purcell, , Kent, D.H. 1960. Senecio squalidus L. the evolution of invasiveness in plants? M.F. & Taylor, G.S. 2009. Molecular in the British Isles. 2. The spread from Proc. Natl. Acad. Sci. U.S.A. 97 (13 ): evidence of hybridization in Florida’s Oxford (1879–1939) . Proc. Bot. Soc. 7043-7050. sheoak ( Casuarina spp.) invasion . Mol. Br. Isl. 3: 375–379. Ecol. 18( 15): 3216–3226. , Enßlin, A., Sandnera, T.M. & Matthiesa, , Lozon, J.D. & MacIsaac, H.J. 1997. D. 2011. Consequences of ex situ , Hoste, I., van Moorsel, R. & Barendse, Biological invasions: are they cultivation of plants: Genetic diversity, R. 2008. Een nieuwkomer in dependent on disturbance? Environ. fitness and adaptation of the sierteeltbedrijven en tuinen: Rev. 5: 131–144. monocarpic Cynoglossum officinale L. Cardamine corymbosa in Nederland in botanic gardens . Biol. Conserv. en België . Dumortiera 93 : 15-24. , Marco, A., Lavergne, S., Dutoit, T. & 144 (1): 272-278. Bertaudiere-Montes, V. 2009. From the , Hulme, P.E. 2011. Addressing the backyard to the backcountry: how , Facon, B., Genton, B.J., Shykoff, J., threat to biodiversity from botanic ecological and biological traits explain Jarne, P., Estoup, A. & David, P. 2006. gardens . Trends Ecol. Evol. 26 : 168- the escape of garden plants into A general eco-evolutionary framework 174. Mediterranean old fields . Biol. for understanding bioinvasions . Trends Invasions 12 (4): 761-779. Ecol. Evol. 21 (3): 130-5. , Keane, R.M. & Crawley, M.J. 2002. Exotic plant invasions and the enemy , Ronse, A. 2011. ‘Botanical garden , Grant, M.L. 2003. A new, purple-leaved release hypothesis . Trends Ecol. Evol. escapes’ in the National Botanic form of Poa annua L. (Poaceae) is a 7: 164–170. Garden of Belgium . Scripta Botanica cryptic weed . Watsonia 24 : 525–526. Belgica 47 in press.

, Sax, D.F. & Brown, J.H. 2000. The Paradox of Invasion . Global Ecology & Biogeography 9: 363-372.

, Simberloff, D. 2009. The role of propagule pressure in biological invasions . Ann. Rev. Ecol. Evol. Syst. 40 (1): 81-102.

, Thompson, J.D. 1991. The biology of an invasive plant: what makes Spartina anglica so successful? Bioscience 41 : 393–401.

, Tiébré, M-S., Vanderhoeven, S., Saad, L. & Mahy, G. 2011. Hybridization and sexual reproduction in the invasive alien Fallopia (Polygonaceae) complex in Belgium . Ann. Bot. 99 : 193-203.

Quentin J. Groom, Anne Ronse and Ivan Hoste National Botanic Garden of Belgium, Domein van Bouchout, Nieuwelaan 38, 1860, Meise, Belgium Tel: +32(0)2 260 0920 Fax: +32(0)2 260 0945 E-mail: [email protected]

Clearing invasive Hedgchium garderianum from a hillside in the Azores (BGCI)

22 BGCI • 2011 • BGjournal • Vol 8 (2) Author: Sarah Reichard

CODES OF CONDUCT TO REDUCE THE THREAT OF INVASIVE SPECIES INTRODUCTION AND SPREAD THROUGH BOTANIC GARDENS

Are botanic gardens sufficiently addressing the issues In 2001 there was a workshop at the Missouri Botanical Garden to develop of invasive plants and can Codes of Conduct help to Codes of Conduct for several horticultural interests, including botanic gardens. The focus attention? process of developing them is discussed in Reichard (2004) and the attendees were largely from the U.S., but included representatives of Australia, New Zealand, and Great Britain. The codes were endorsed by the American Public here is increasing knowledge of also found to play a “ considerable role in Garden Association and several individual the environmental and economic the synanthropic flora of Central Europe in gardens. Gardens began implementation, Tharm caused by invasive species the last 200 years ” (Galera and Sudnick- using a broad group of stakeholders from to native species and ecosystems (Mack Wójcikowska 2010). Hulme (2011) within and outside the institution. Most et al ., 2000, Pimental et al ., 2000). Those implicates gardens for the early found the framework the Codes provided who place a high value on the protection introduction and cultivation of invasive to be a helpful way to address practices of wild lands are concerned that plants throughout the world. While all of throughout the institution, not just the introduced plants are causing those these papers can be examined for flaws in collections. The codes are summarized in areas to be irreversibly altered. While methods, and an argument can be made Table 1, but can be read in entirety, along many agricultural weeds have arrived for including potentially invasive species in with the workshop proceedings in accidentally, the majority of invasive botanic garden collections for a variety of Reichard et al . (2002). plants invading natural areas were reasons, including education about their introduced for horticultural purposes invasiveness, (see Sharrock in press for In the United Kingdom, the Department (Gordon and Thomas, 1997, Reichard, more), it is a subject that should be of Environment, Food, and Rural Affairs 1997, Reichard and White, 2001). Plant examined by gardens individually and (DEFRA) later published similar exploration and introduction is part of discussed collectively. Horticultural Codes of Practice (DEFRA, many botanic gardens’ missions, and 2005). While many of the Codes of collection displays are important to all Hulme (2011) points out that while efforts Practice were similar to the Codes of gardens. have been made to develop voluntary Conduct developed in the U.S., they did Codes of Conduct, or best management not focus on botanic gardens and only a Botanic gardens share the practices for horticultural interests, few of the practices specifically included including botanic gardens, these Codes ‘botanic collections’ as their targets. r“esponsibility of ensuring that have been ineffective. He measures their However, despite this, some of the our activities do no harm to wild effectiveness, in part, as the number of practices that did not name botanic United States (U.S.) gardens that have gardens as a target are still relevant and lands. formally endorsed the codes. There are some did specify they were relevant to ” many gardens that are actively all horticultural interest groups. Recently, botanic gardens have been implementing measures consistent with criticized for their contributions to the the Codes that have not formerly The Council of Europe has also introduction and spread of invasive plants. endorsed them, but it is hard to argue developed Codes of Conduct for the Dawson et al. (2008), using a garden in that botanic gardens are sufficiently horticultural industry (Heywood and Tanzania as a case study, theorized that addressing their role in the introduction Brunel, 2008) but specifically stated that, tropical gardens were responsible for the and spread of invasive plants. This is an while the recommendations may be distribution, naturalization, and spread of area of conservation that deserves more relevant to botanic gardens, the codes non-native plants. Botanic gardens were of our attention. were not addressing gardens. They point

BGCI • 2011 • BGjournal • Vol 8 (2) • 23-25 23 Lantana camasa invading Butea monosperma relict forest in Pakistan (Joachim Gratzfeld) out that many European gardens are botanic gardens are educating the public , Galera, H. and Sudnick-Wójcikowska, already working in partnerships and about the importance of responsible B. 2010. Central European botanic some relevant guidelines exist, including stewardship of our Earth. gardens as centres of dispersal of alien the International Plant Exchange plants . Acta Societatis Botanicorum Network’s (IPEN) guidelines on non- References Poloniae. 79 : 144-156. commercial exchanges of plant material, although the purposes of IPEN are much , Dawson, W., Mndolwa, A.S., Burslem, , Gordon, D. and Thomas, K. 1997. broader than invasive species i. D., Hulme P.E. 2008. Assessing the Florida’s invasion by nonindigenous risks of plant invasions arising from plants: history, screening, and The guidelines from the three Codes of collections in tropical botanical regulation . In Simberloff, Schmitz, and Conduct mentioned above are gardens . Biodiversity Conservation 17 : Brown (eds.) Strangers in Paradise . summarized in Table 1. 1979-1995. Island Press. pp. 21-37.

It is recommended that all gardens should , Department for Environment, Food, and , Heywood, V. and Brunel S. 2008. visit the sites and documents listed as Rural Affairs (DEFRA) (2005). Helping to Code of conduct on horticulture and resources and consider implementing the prevent the spread of invasive non- invasive alien plants . Nature and Codes of Conduct that are appropriate to native species: horticultural code of Environment No. 155. Strasbourg, their institution. The reward will be a practice . (http://www.botanicgardens.ie Council of Europe Publishing deeper involvement in global conservation /gspc/pdfs/defra%20code%20of%20 and the knowledge that once again, practice.pdf)

24 BGCI • 2011 • BGjournal i Codes of Conduct for botanic gardens in Europe are presently under development. See Heywood, p. 26-28 of this issue. For further information about IPEN, visit: http://www.bgci.org/resources/ipen/ Summarized Code 1234

Assess risk of new species prior to introduction X Identify current invaders, remove when appropriate XXX Identify & promote safe alternative species XX Become partners with other organizations and stakeholders to prevent and manage invasions XX Education – public and professional outreach & formal education XX Participate in early warning & monitoring programs to detect new invaders X Enforce and respect legislation, help create when appropriate XXXX Examine collection policies, as well as do an institution wide-assessment X Control invasive plants in natural areas managed by the garden using best practices XXX Exchange invasive plants for non-commercial purposes with caution X* Beware of hitchhiking organisms on plants and soil, use good production practices XXX Ensure correct labeling of names and potential harm to the environment XX Know the invasive ability of what you are specifying in landscapes, books and articles X Dispose of plant waste responsibly XXX Know what you are buying X Avoid planting invasive plants in large scale public plantings X Beware of potential distribution changes due to future climate change X *The Council on Europe considers this addressed by the IPEN

Table 1. Summarizing the United States (1), Great Britain – Botanical Collections (2), Great Britain – All (3) and Council of Europe General Codes (4). The goals and audience of the three efforts were not identical; complete agreement is not expected.

, Hulme, P.E. 2011. Addressing the , Reichard, S. 2004. Conflicting values Sarah Reichard, Ph.D. threat to biodiversity from botanic and common goals: codes of conduct University of Washington Botanic gardens . Trees in Ecology and to reduce the threat of invasive species . Gardens Evolution 26 : 168-174. Weed Technology 18 :1503-1507. University of Washington, Box 358010, Seattle , Mack, R.N., Simberloff, D., Lonsdale, , Sharrock, S. in press. The biodiversity Washington 98195-8010 W.M., Evans, H., Clout, M. and Bazzaz, benefits of botanic gardens . Trends in United States of America F. 2000. Biotic invasions: causes, Ecology and Evolution. Email: [email protected] epidemiology, global consequences, and control . Issues in Ecology 5: 1-22.

, Pimental, D., Lach, L., Zuniga, R.and Morrison D. 2000. Environmental and Economic Costs of Non-Indigenous Species in the United States . BioScience 50 : 53-65.

, Reichard, S.H. 1997. Preventing the introduction of invasive plants. In Luken, J. and J. Thieret (eds) Assessment and management of plant invasions . Springer-Verlag: New York. pp. 215-227.

, Reichard, S.H. and White P. 2001. Horticulture as a pathway of invasive plant introductions in the United States . BioScience 51 : 103-113.

, Reichard, S.H., Randall, J.M., Raven, P.D., Raven, P.H. and White P.S. 2002. Linking ecology and horticulture to prevent plant invasions . (http://www.centerforplantconservatio n.org/invasives/CodesN.asp) Interpretation sign at the Chicago Botanic Garden (BGCI)

BGCI • 2011 • BGjournal • Vol 8 (2) 25 Author: Vernon H. Heywood

A CODE OF CONDUCT ON INVASIVE ALIEN SPECIES FOR EUROPE’S BOTANIC GARDENS

Voluntary codes of conduct are a valuable tool in dealing with the threats of invasive species and should be widely adopted by botanic gardens. A code for

European botanic gardens is being prepared by the governments and the horticultural industry and trade (importers, traders, Council of Europe and BGCI. nurseries, garden centres, aquarists, landscape architects, managers of public or private areas. The aims of the Code are (1) to enlist the co-operation of Introduction species’. Separately, as part of its work the horticultural industry and trade in in promoting actions to avoid the raising awareness of this topic among t is widely recognized that ornamental intentional introduction and spread of professionals; (2) preventing the spread horticulture has been the main pathway alien species and prevent their of invasive alien species already present Iof plant invasions and that most accidental introductions and to build an in Europe; and (3) preventing the invasive plants have been introduced by information system the Bern Convention introduction of possible new invasive nurseries and botanic gardens or by Group of Experts on IAS of the Council alien species into Europe. Some individuals (Reichard and White, 2001). of Europe had plans to prepare a code of countries have prepared codes of Botanic gardens, especially those located conduct for botanic gardens. A conduct for IAS such as the United in tropical countries, have often been collaboration between the Council of Kingdom’s Horticultural Code of Practice implicated as the source of such Europe and BGCI was therefore aimed at preventing the spread of alien invasions (Dawson et al ., 2008; Hulme, proposed and work is now in hand for invasive species (DEFRA, 2005), a code 2011) although it is not always easy to the two organizations to prepare jointly a of conduct for gardeners and designers establish the full facts (Galera, H. and Code of Conduct for Botanic Gardens that has also been developed in Sudnik-Wójcikowsja, 2010). Given that and Invasive Alien Species. BGCI is Germany 2 and a national code for the Invasive Alien Species (IAS) are widely liaising on this with the European horticultural sector that is under regarded as one of the main threats to Botanic Gardens Consortium, and the development in Belgium 3. biodiversity today, it is incumbent on IUCN Species Survival Commission botanic gardens to consider what actions Invasive Species Specialist Group (ISSG) Very few codes of conduct on they can take to prevent such invasions has also been invited to participate in or to deal with existing ones. Amongst the drafting of the Code. “IAS specific for botanic gardens the tools that may be deployed to combat have been prepared. IAS are voluntary codes of conduct. Existing codes of conduct ” The desirability of preparing a code of A number of codes of conduct for In Europe, a German-Austrian Code of conduct for botanic gardens and dealing with IAS have been published Conduct for the cultivation and invasive alien species has been raised at both in Europe and elsewhere. In management of invasive alien plants in several meetings, most recently at Europe, the Council of Europe in botanic gardens has been developed EuroGard V in Helsinki (2009) where a collaboration with the European and (Kiehn et al ., 2007) and the National resolution was passed recommending Mediterranean Plant Protection Botanic Gardens of Ireland has a draft inter alia that botanic gardens should Organization (EPPO) has produced a Code of Conduct on the management of ‘develop and implement guidelines, Code of Conduct on Horticulture and actual or potentially invasive species. Codes of Conduct, and appropriate Invasive Alien Plants (Heywood and In the United States, a Voluntary Code of practices to prevent the spread of alien Brunel, 2009, 2011 1), aimed at Conduct for Botanic Gardens and

1 EPPO / Council of Europe Workshop ‘Code of conduct on horticulture and invasive alien plants’ 2009-06-04/05, Ski (NO) http://archives.eppo.org/MEETINGS/2009_conferences/conf_codeofconduct.htm#pres 2 Zentralverband Gartenbau (2008): Umgang mit invasiven Arten. Empfehlungen für Gärtner, Planer und Verwender. Zentralverband Gartenbau (Berlin), 37 S. 3 AlterIAS (IAS for Invasive Alien Species) is a communication project which aims at educating the horticultural sector on the invasive plants issue: http://www.alterias.be/. Arboreta (and one for Nursery although there may be a general created with the stakeholders through Professionals) arose out of a workshop awareness of the problems of IAS, few if workshops and other approaches. ‘Linking Ecology and Horticulture to any policies are in place. Consequently The Botanic Gardens Code will likewise Prevent Plant Invasions’ that was held at the background and raison d’être of the be submitted for approval to the Standing the Missouri Botanical Garden in St. Louis precepts of the proposed Code will need Committee and it is expected that the in December 2001 (Fay et al ., 2001). A to be given and guidance provided on implementation strategy at the garden follow-up workshop was held in 2002 at where further information and level will be developed by BGCI and the Chicago Botanic Garden (Fay et al ., explanations can be found. The relevant European Botanic Gardens Consortium. 2002). Several US botanic gardens have international and national legislation and endorsed the Voluntary Codes. A initiatives that botanic gardens need to be The proposed Code for botanic gardens detailed review of how Canada, Mexico, aware of are many and varied and so it will be voluntary in the sense that the and the United States are confronting the would be naïve to assume that such parties adopting it will not have to sign challenges posed by invasive plants was knowledge is widespread. The challenge up to any legislation; rather, they will the theme of the Weeds Across Borders will be to address these points and get the follow the principle of self-regulation and (WAB) 2010 conference (Rindos, 2011). balance right. it is hoped that most European botanic gardens will sign up to the actions and The context A Code of Conduct must be recommendations made in the Code. This does not mean, however, that In Europe, it has been estimated that 80 “suitable for implementation by voluntary codes such as this will have no per cent of invasive alien plants are all gardens, regardless of size legal implications or lack effective means introduced for ornamental and agricultural of enforcement (Webb, 1999). There is purposes (Hulme, 2007). On the other and resource base. some evidence to suggest that such hand, although the biological, economic ” high-level ‘soft law’ instruments can be and social threats posed IAS are now effective (Shine et al ., 2010). On the widely recognized by the conservation How to make it work other hand, such codes or guidelines community, in Europe there is a general have no specific targets or time-frame lack of perception of these threats and Publication of a Code is only the first step and their effectiveness depends largely even a certain degree of scepticism about in a process. For it to be successfully on how well they are promoted (Dehnen- their significance (Brundu et al ., 2011). implemented, a strategy for promoting it Schmutz and Touza, 2008). Moreover, a There is no European level regulation on will be needed as in the case of the system that is built on voluntary invasive alien plants although the EC Council of Europe/EPPO Code of undertakings by member states and adopted a Communication presenting Conduct on Horticulture and Invasive voluntary codes of conduct would only policy options for an EU Strategy on Alien Species (Burundu et al ., 2011) which be as effective as the weakest link in a Invasive Species in December 2008. was endorsed by the Standing Committee chain (Kettunen et al ., 2008). of the Convention on the Conservation of Likewise at national level in Europe, the European Wildlife and Natural Habitats in The preparation of the Code of Conduct situation regarding the regulation of IAS November 2008 with the should provide botanic gardens with a is extremely diverse. In the various recommendations that the contracting stimulus to develop their education and European countries a complex, countries draw up national codes of outreach policies on invasive alien fragmented and continually developing conduct on horticulture and invasive alien species so as to better inform the public network of legislative instruments and plants taking into account the European of the issues surrounding these species regulations is in operation aimed at Code of Conduct. A dialogue was and the risks they pose to biodiversity. preventing or prohibiting the introduction and spread of non-native species that pose a threat to native species and ecosystems and to agriculture, fisheries, forestry and horticulture (Miller et al ., 2006).

Preparing the Code

It would be relatively simple to prepare and agree a list of actions and good practice to be followed by botanic gardens in dealing with IAS but we have to take into account the very wide range of perceptions and experience in Europe’s botanic gardens. While some gardens are well informed of the issues and actively engaged in policies and actions to prevent their introduction and diffusion and are engaged in control measures, in others, Carpobrotus invasive at Cap de Favaritx, Menorca, Spain (V. H. Heywood)

BGCI • 2011 • BGjournal • Vol 8 (2) 27 Botanic gardens are uniquely suited to , Galera, H., and Sudnik-Wójcikowsja, , Reichard, S.H., and White, P. 2001. spread such a message and it goes B. 2010. Central European botanic Horticulture as a pathway of invasive without saying that compliance with the gardens as centres of dispersal of alien plant introductions in the United Code would be a necessary basis from plants . Acta Soc. Bot. Pol. 79 :147- States . BioScience 51 :1103–1113. which to start. 156. , Rindos, E. (ed.). 2011. Plant Invasions: References , Heywood, V.H. and Brunel, S. 2009. Policies, Politics, and Practices . Code of Conduct on Horticulture and Proceedings of the 2010 Weeds , Brundu, G., Brunel, S., and Heywood, Invasive Alien Plants . Nature and Across Borders Conference, 1–4 June V. 2011. The European Code of Environment No. 155. Strasbourg, 2010. National Conservation Training Conduct on Horticulture and Invasive Council of Europe Publishing. Center, Shepherdstown, West Virginia. Alien Plants . In: Rindos, E. (ed.), Plant Bozeman, Montana: Montana State Invasions: Policies, Politics, and , Heywood, V.H. and Brunel, S. 2011. University, Center for Invasive Plant Practices. Proceedings of the 2010 Code of Conduct on Horticulture and Management. Weeds Across Borders Conference, Invasive Alien Plants . Illustrated 1–4 June 2010, Pp. 32–26. National version. Nature and Environment No. , Shine, C., Kettunen, M., Genovesi, P., Conservation Training Center, 162. Strasbourg, Council of Europe Essl, F., Gollasch, S., Rabitsch, W., Shepherdstown, West Virginia. Publishing. Scalera, R., Starfinger, U. and ten Bozeman, Montana: Montana State Brink, P. 2010. Assessment to support University, Center for Invasive Plant , Hulme, P.E. 2007. Biological Invasions continued development of the EU Management. in Europe: Drivers, Pressures, States, Strategy to combat invasive alien Impacts and Responses . In: Hester, R. species. Final Report for the European , Dawson, W., Mndolwa, A.S., Burslem, and Harrison, R.M. (eds.), Biodiversity Commission . Institute for European D. and Hulme, P.E. 2008. Assessing Under Threat . Issues in Environmental Environmental Policy (IEEP), Brussels. the risks of plant invasions arising from Science and Technology, 2007, pp. collections in tropical botanical 55-79, 25 Royal Society of Chemistry, , Web, K. 1999. Voluntary initiatives and gardens . Biodiversity & Conservation Cambridge. the law . In: Gibson, R. (ed.), Voluntary 17 :1979–1995. Initiatives: The New Politics of , Hulme, P.E. 2011. Addressing the Corporate Greening Pp. 32–50. , DEFRA. 2005. Helping to prevent the threat to biodiversity from botanic Peterborough, Ontario: Broadview. spread of invasive non-native species . gardens . Trends in Ecology & Horticultural Code of Practice, Evolution 26 : 168 –174. The Code is available in English, French http://www.defra.gov.uk/wildlife- and Spanish, in hard copy and on the countryside/non-native/pdf/non-native , Kettunen, M., Genovesi, P., Gollasch, Internet: cop.pdf. S., Pagad, S., Starfinger, U., ten Brink , P., and Shine, C. 2008. Technical http://www.coe.int/t/dg4/cultureheritage/ , Dehnen-Schmutz, K., and Touza, J. support to EU strategy on invasive nature/Bern/IAS/default_en.asp [English] 2008. Plant invasions and ornamental species (IS)—assessment of the horticulture: pathway, propagule impacts of IS in Europe and the EU http://www.coe.int/t/dg4/cultureheritage/ pressure and the legal framework . In: (Final module report for the European nature/bern/ias/default_FR.asp [French] Teixeira da Silva JA (ed.) Floriculture, Commission) . Institute for European ornamental and plant biotechnology: Environmental Policy (IEEP), Brussels http://www.coe.int/t/dg4/cultureheritage/ advances and topical issues . Global (40pp. + Annexes, May 2008 (DG ENV nature/bern/ias/CODIGO%20HORTICUL Science Books, Isleworth, UK, contract)). TURA%20MAIL.pdf [Spanish] pp. 15–21. , Kiehn, M., Lauerer, M., Lobin, W., Czech and Polish versions have also , Fay, K., Fay, K.C. et al . 2001. Schepker, H., and Klingenstein, F. been prepared. Proceedings of the Workshop at the 2007. Grundsätzen im Umgang mit Missouri Botanical Garden, St. Louis, invasiven und potentiell invasiven Vernon H. Heywood Missouri, 1–4 December 2001 . Pflanzenarten in Botanischen Gärten Emeritus Professor http://www.centerforplantconservation des Verbandes Botanischer Gärten School of Biological Sciences .org/invasives/Download%20PDF/ und der AG Österreichischer University of Reading, UK Proceedings_FINAL.pdf. Botanischer Gärten . Gärtnerisch- Email: [email protected] Botanischer Brief 169 (4):39–41. , Fay, K., Fay, K.C. et al . 2002. Proceedings of the Workshop II at the , Miller, C., Kettunen, M., and Shine, C. Chicago Botanic Garden, Chicago, 2006. Scope options for EU action on Illinois, 31 October 2002. invasive alien species (IAS). Final http://www.centerforplantconservation report for the European Commission . .org/invasives/Download%20PDF/ Institute for European Environmental CBG_Proceedings.pdf. Policy (IEEP), Brussels, Belgium.

28 BGCI • 2011 • BGjournal • Vol 8 (2) Authors: Olivier Filippi and James Aronson

USEFUL BUT POTENTIALLY INVASIVE PLANTS IN THE MEDITERRANEAN REGION: WHAT RESTRICTIONS SHOULD BE PLACED ON THEIR USE IN GARDENS?

Gardens and other amenity plantings are expanding economies, as well as for native fauna, flora, biotic communities, and rapidly throughout the Mediterranean region - a simple ecosystems. Decisions regarding the choice of plant material to be used in protocol, based on relevant information, may help gardens and amenity areas are therefore a growing cause for concern. determine which plants should be used, and which Consideration of both the positive and the negative aspects of the various plant should be avoided. species that can be used horticulturally is required.

What is an invasive plant?

Introduction environmental and cultural functions. According to Richardson et al . (2000), Whereas they are perceived by the invasive species are exotic species that n the Mediterranean region as a whole, general public as places of ‘Nature’, they overcome successive barriers limiting rising standards of living and can be seriously harmful for the their reproduction, naturalization, and Iexpanding urbanisation are leading to environment because of their heavy dispersal, allowing them to spread in rapid extension of land areas devoted to consumption of water and the their new area of introduction. However, gardens and other planting areas. This widespread application of pesticides, the term itself of invasive species is entails complex environmental and fertilisers, and weed killers. They can confusing: a species can never be cultural consequences that should be also be the starting point for the invasive in and of itself; only a population studied carefully since gardens and dissemination of exotic invasive plants of a species can be invasive, in a given other amenity planting areas have both involving risks for human health, and place and at a given time (Colautti & MacIsaac, 2004). For some plants deemed invasive, there may also be uncertainty, at the local level, regarding the status of species or subspecies considered “native” (Beisel & Lévêque, 2009), especially in the context of the Mediterranean Basin with its complex history of intermingling flora and fauna, much influenced and mediated by human choices and activities. This sometimes hinders conservationists and ecologists seeking to dialogue with gardeners, horticultural professionals and landscapers in order to define which invasive plants to avoid when planting.

Indeed, in order to limit the spread of noxious invasive plants, such as Ice plant ( Carpobrotus spp., Aizoaceae; Figure 1), many lists of species have been created in different countries of Figure 1: An Ice plant ( Carpobrotus spp.) invasion on a coastal dune in Corsica (O. Filippi). southern Europe.

BGCI • 2011 • BGjournal • Vol 8 (2) • 29-33 29 Invasive plant to evaluate for garden use Decision-making protocol Problems Impact on for health Do not cultivate To classify invasive plants for use or not human health? Ex: Ambrosia artemisifolia to use in gardens and amenity plantings, we offer a decision-making protocol No problems 1: Impacts for health (Figure 2) with the following steps: a candidate species’ potential negative Impact on Weak impacts in the introduction zone are the economy Plantation possible or natural But keep under observation studied followed by an assessment of ecosystems? Ex: Pittosporum the risk of the species spreading outside of the planting site; then the species’ Medium or high potential positive aspects in a horticultural setting are also considered. Many Habitat type(s) Do not cultivate For each candidate species, answers to where the plant is Ex: Cortaderia sellonoana these successive questions can result in invasive? three types of decisions: 1) use of the 2: Habitat and One specific plant should be proscribed regardless of mode of dispersal habitat type (ex: the planting site (dark grey in Figure 1); dune, ripisylve) 2) the species can be grown in any zone, Long distance Mode of Do not cultivate but the plant should remain under dispersal? Ex: Baccharis halimifolia observation in case conditions change (e.g. due to global warming) and lead to a revision in status (light grey); 3) the Short distance Helps reduce species can be grown only outside of the environmental impact of Plantation possible zones at risk defined for this species plantations except in vulnerable zones (white). Environmental (Careful labelling in nursery benefit? required) Ex: Lippia canescens 1) Evaluation criteria of invasive plants No environmental Invasive plants can have several types of 3: Benefits benefits Plantation possible negative impacts (Heywood & Brunel, Major apart from vulnerable 2009), including those impinging directly Cultural, economic interest zones (Careful labelling in on human health, those affecting or other value? nursery required) Ex: Acacia deslbata economic activities and those affecting (only grafted varieties native biodiversity and the functionality No major allowed) interest of natural or semi-natural ecosystems. Albeit no tool has yet been Do not cultivate internationally recognized for the Ex: Oenothera speciosa assessment of the negative impact of invasive species on native biodiversity Figure 2: A decision-making protocol to help determine which types of restriction to impose for any given and ecosystems, several approaches non-indigenous species under consideration for use in gardens or amenity plantings. have been suggested (Vitousek et al ., 1987; Hulme et al ., 2007; Parker et Gardens and amenity that have as their main defect that they al ., 1999). Here we adopt the Belgian p“lantings can be the starting are not considered “native” (Gould, protocol for measuring the impact of 1997), may inflate the lists of unwanted invasive plants (ISEIA, 2007) (see Figures point for dissemination of exotic or forbidden plants in gardens and 3 and 4). invasive plants. amenity plantings and unleash negative reactions from horticulture and When evaluating invasive ” landscape professionals. To progress on Unfortunately, many of these lists, even these sensitive issues – which are “plants, we suggest focusing on those created by official environmental sometimes strongly marked by the positive and negative aspects protection agencies, are based on emotional and subjective dimensions inconsistent criteria (Heywood & Brunel, (Webb, 1985; Wilcove et al ., 1998) – of the species rather than on 2009), thereby contributing to confusion particular attention should be paid to the place of origin. and preventing well-meaning choice of targeted species and how recommendations from being decisions are made (Ewel et al ., 1999; ” implemented. Moreover, these lists are Parker et al. , 1999). In the following In which cases should a potentially often elaborated at different spatial section, a protocol is described to aid in invasive plant species be subject to scales, e.g. national or regional, which decision-making regarding which plant complete, or partial, proscription? In may generate conflicting species to use freely - or to avoid at all case of partial proscription, which uses recommendations. The confusion of costs - in gardens and amenity plantings can be allowed, without entailing any species genuinely noxious and those across a range of situations. environmental risk? In order to evaluate

30 BGCI • 2011 • BGjournal • Vol 8 (2) the risk of invasion by a cultivated plant that might ‘escape’ from the site where it is intentionally planted, we first consider in what type of environment the plant is potentially invasive. In other words, is it a “generalist invasive” or a “specialist invasive” (Barbault & Teyssèdre, 2009)? A generalist invasive species is able to colonize many different environments, including natural, semi-natural, or human-dominated (e.g. Uruguayan Pampas grass, Cortaderia sellowiana (Schult. & Schult. f.) Asch. & Graebn. (Müller, 2004). A specialist invasive by contrast only colonizes one particular type of ecosystem, such as coastal dunes or riparian forests – both of which are in fact among the most sensitive ecosystems to invasive plants in the Mediterranean region (Chytry et al ., 2009; Vilà et al ., 2008).

If it is, or suspected to be, noxious, the planting of a generalist invasive plant Figure 3: Hyparrhenia hirta , which is considered native in France, is deemed exotic and potentially invasive in Spain should be proscribed in all cases, since (O. Filippi). all – or almost all - gardens constitute zones at risk from which such invasive & Fahrig, 2000), refers to the likelihood reduce the ecological footprint of species can escape. In contrast, for that a species with invasive potential traditional gardens and amenity plantings specialist invasive plants, the definition may succeed in migrating from one where the plant may be used. This can be of zones at risk where the planting ecosystem type to another within a given done according to three parameters, should be proscribed depends on the landscape (Taylor et al ., 2006) (Figure 5). namely water consumption, chemical ecological connectivity between the inputs required (fertilizers, weed killers, planting site and the environment where Regarding the positive aspects of a insecticides, and fungicides, etc.), and fuel the plant is potentially invasive. This horticultural plant, whether it is native or consumption related to maintenance notion of ecological connectivity, which exotic, our protocol calls for analyzing operations requiring engine tools: can be structural and/or functional how best to use the plant in order to take mowers, hedge-trimmers, brush cutters, (Metzger & Décamps, 1997; Tichendorf advantage of its attributes in order to waste removal, etc.

2) Bibliographic database on plant species Another tool is required for using this decision-making protocol to help identify and gather the necessary information in one standardized evaluation document, consisting of a database on the risks and advantages of invasive, or potentially invasive, plants used in gardens and amenity plantings. In order to reduce the risk of errors related to an overly narrow perception (Pyšek et al ., 2009), we suggest that the database should be established by an interprofessional group including scientists and landscape professionals. This database should identify its different sources (bibliographies, experts’ interviews or authors’ personal observations). The European Botanic Gardens Consortium for example, could and should play a major role in Figure 4: Medicago arborea , a highly ornamental but colonizing Mediterranean shrub, is expanding its range from developing, updating, and implementing east to west and is now considered a planta non grata by some conservationists in southern France (O. Filippi). this database. Head gardeners,

BGCI • 2011 • BGjournal • Vol 8 (2) 31 new tool we offer will contribute to the debate on the issue of holistic assessment of invasive plants, some of which may be valuable for Mediterranean horticulture. We assert that a comprehensive analysis is required to lead to collective decisions, based on a consistent method. Only in this way will it be possible to bring together gardeners, nurserymen, landscape planners and botanic gardens, rarely consulted in this regard and yet key players, in search of a consistent policy aimed at limiting the spread of noxious invasive plants. We emphasize that there is a real risk of seeing these players reject outright any recommendations – or even legislation – which may seem arbitrary or lacking in a robust scientific basis.

Concurrently, the protocol we propose has potential use in the broader context of ecosystem management, conservation ecology, and restoration Figure 5: Pennisetum villosum and Oxalis pes-caprae have long distance propagation modes, enabling them ecology. Happily, botanical gardens to escape readily from planting sites (O. Filippi). around the world are getting much more active in these areas (Hardwick et al ., horticulturists, and botanists of botanic these species might be possible should 2011) and the new list of Targets of the garden staff are perhaps the most be given special attention, in order to Global Strategy for Plant Conservation knowledgeable experts anywhere and avoid the plants at issue spreading into (http://www.cbd.int/gspc/targets.shtml) should participate in all collective efforts areas or ecosystems where they may also suggests that the development of a undertaken to evaluate potentially become noxious. holistic, decision-making protocol invasive species in an holistic fashion concerning invasive and potentially (Figure 6). Conclusions invasive plants is timely.

As the ecological footprint of Prevention and precaution remain vital to Acknowledgements help limit the environmental risk related a“menity planting is increasing to the introduction of invasive plants Many thanks to Bérengère Merlot (CEFE, rapidly in the Mediterranean (Ewel et al. , 1999; Hulme et al ., 2007; CNRS) for her help with the manuscript, Gasso et al ., 2009). We hope that the and to Charlotte Yelnik. region, the choice of well-adapted exotics can be very useful. ” Discussion

Following test application on twenty exotic species used horticulturally in the Mediterranean region (Filippi & Aronson, 2010), our decision-making protocol clearly allows candidate species to be classified according to which of the three types of use restrictions to recommend. However, the reliability of this protocol should be validated with many more examples. The decision-making protocol can establish, at least for some specialist invasive plants with a short- distance spreading mode, the possibility of planting in low-risk areas. The process Figure 6: Phyla canescens is a cosmopolitan ground-cover species that is considered exotic in France. of demarcating the areas where planting However, the use of this plant allows savings in irrigation water, herbicides and mowing (O. Filippi).

32 BGCI • 2011 • BGjournal • Vol 8 (2) References J., Holmes, P.M., Mabberley, D., , Richardson, D.M., Pysek, F.D., Mackenzie, A., Magdelena, C., Marrs, Rejmánek, M., Barbour, M.G., Panetta, , Barbault, R. and Teyssèdre, A. 2009. R., Mills, A., Ramsay, M., Smith, P., F.D. and West, C.J. 2000. La victime était le coupable ! Dossier Taylor, N. Trivedi, C., Way, M., Whaley, Naturalization and invasion of alien pour la Science 65 : 56-61. O. and Hopper, S.D. 2011. Defining plants: concepts and definitions. the Role of Botanic Gardens in the Divers. Distrib. 6: 93-107. , Beisel, J.-N. and Levêque, C. 2009. Science and Practice of Ecological Les eaux douces, propices aux Restoration. Conservation Biology 25 : , Taylor, P.D., Fahrig, L. and With, K. A. invasions? Dossier pour la Science 65 : 265–275. 2006. Landscape connectivity: a return 26-30. to the basics in: Connectivity , Heywood V. and Brunel S. 2009. Code Conservation (eds. K.R. 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Lloret, F., Sanz-Elorza, M., Sobrino, E. scientifiques du Museum National Quantifying threats to imperilled and Vilà M. 2009. Exploring species d’Histoire Naturelle. species in the United States . attributes and site characteristics to Bioscience 48 : 607-615. assess plant invasions in Spain . Divers. , Parker, I.M., Simberloff, D., Lonsdale, Distrib. 15 : 50-58. W.M., Goodell, K., Wonham, M., O. Filippi (Corresponding author) Kareiva, P.M., Willimason, M.H., Von Pépinière Filippi , Gould, S. 1997. An evolutionary Holle, B., Moyle, P.B., Byers, J.E. and R.D. 613 perspective on strengths, fallacies and Goldwasser, L. 1999. Impact: toward a 34140 Mèze confusions in the concept of native framework for understanding the France plants . Washington, D.C., Nature and ecological effect of invaders . Biol. [email protected] Ideology, Dumbarton Oaks Research Invasions 1: 3-19. Library and Collection. J. Aronson , Pyšek, P., Hulme, P. and Nentwig, W. 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BGCI • 2011 • BGjournal • Vol 8 (2) 33 RESOURCES

Invasive and Introduced Plants ‘An interesting and maintenance, while helpful, “at a and Animals and much- glance” boxes depict shapes, sizes, best Human Perceptions, Attitudes and needed book locations, and most attractive features of Approaches to Management. that tackles an each native alternative. Editors: Ian D. Rotherham and important Robert A. Lambert aspect of invasive alien species: how they ISBN: 978-1889538778 are perceived, valued and judged by Published by: Brooklyn Botanic Garden, This book addresses the broader context humans. The volume draws together a 2011 of invasive and exotic species, in terms of broad range of fascinating case studies www.bbg.org the perceived threats and environmental and is very thought-provoking. A must for concerns which surround alien species any serious invasion ecologist.’ and ecological invasions. As a result of (Robert A. Francis, King's College Invasive Alien Species: unprecedented scales of environmental London, and Secretary of the British A Toolkit of Best Prevention change, combined with rapid Ecological Society Invasive Species and Management Practices globalisation, the mixing of cultures and Special Interest Group). Edited by R Wittenberg, and diversity, and fears over biosecurity and M.J.W. Cock bioterrorism, the known impacts of ISBN 9781849710718 particular invasions have been Published by Earthscan Human activities have catastrophic. However, as several www.earthscan.co.uk contributed to the distribution chapters show, reactions to some exotic of many plant, animal and species, and the justifications for microbial species to parts of interventions in certain situations, Native Alternatives to Invasive Plants the world where they are not including biological control by introduced (Brooklyn Botanic Gardens Guides for native. This spread of alien natural enemies, rest uncomfortably with a Greener Planet) species can have devastating social reactions to ethnic cleansing and Author: C. Colston Burrell; Editors: Janet consequences on native biodiversity. persecution perpetrated across the globe. Marinelli and Bonnie Harper-Lore. Examples include alien mammals The role of democracy in deciding and consuming native vegetation and alien determining environmental policy is The biggest insects spreading viruses, as well as another emerging issue. In an increasingly enemy of any plants such as water hyacinth, which has multicultural society this raises huge garden is not a caused major problems to waterways questions of ethics and choice. At the pest, disease, or when introduced from South America. same time, in order to redress major poison. It’s any CABI’s goal is to improve prevention and ecological losses, the science of plant with tougher management of biological invasions, and reintroduction of native species has also survival skills than this book represents a key outcome. come to the fore, and is widely accepted the plants it It has been assembled by a team of by many in nature conservation. However, competes with. international experts. Features include: with questions of where and when, and This book case studies from around the globe, with with what species or even species provides a guide some emphasis on islands, a focus on analogues, reintroductions are to the native biodiversity, but with some consideration acceptable, the topic is hotly debated. plants that can replace the top 100 most of traditional agriculture and forestry, Again, it is shown that many decisions are unwelcome perennials, grasses, vines, advice on national management plans, based on values and perceptions rather shrubs, and trees in the USA. While including risk analysis. than objective science. Including a wide replacing the invaders, the beautiful, range of case studies from around the hardy native plants described here also Published by CAB International, 2001 world, this book raises critical issues to attract native birds and butterflies. Word- ISBN: 978-0851995694 stimulate a much wider debate. and-picture guides provide tips on care http://bookshop.cabi.org

34 BGCI • 2011 • BGjournal • Vol 8 (2) • 34-35 Websites and on-line resources • Datasheets on over 1500 invasive species and animal diseases • Basic datasheets on further species, CABI - Invasive Species Compendium countries, habitats and pathways • Bibliographic database of over 65,000 An encyclopaedic resource that draws records (updated weekly). together scientific information on all aspects of invasive species. The Compendium is available at: data and information on IAS around the Invasive species are a major threat to the www.cabi.org/isc world. Computer-based information global economy and the environment, systems like those in the GISIN present costing billions of dollars to control each specific information to help detect, rapidly year. The Invasive Species Compendium The Global Invasive Species Database respond to, and control IAS. GISIN data is an online, comprehensive providers such as the Invasive Species encyclopaedic reference work covering Specialist Group’s Global Invasive recognition, biology, distribution, impact Species Database and management of the world’s invasive (www.issg.org/database ), the U.S. plants and animals. National Institute of Invasive Species Science ( www.niiss.org ), and the Delivering Alien Invasive Species Inventories for Europe (DAISIE) project (www.europe-aliens.org ), create common gateways to search, share, and compare IAS information from around the globe. The Global Invasive Species Database While varying in scope and administrative (GSID) aims to increase awareness about origin, these initiatives are united by a invasive alien species and to facilitate common set of principles. They seek to effective prevention and management make IAS data freely and quickly available activities. It is managed by the Invasive to a broad population of consumers Developed by CABI, with support from a Species Specialist Group (ISSG) of the around the world. To achieve this, they consortium of partners, this resource will Species Survival Commission of the participate in the development and be the most extensive and authoritative IUCN-World Conservation Union. The promotion of IAS information compilation on the subject in the world. GISD was developed as part of the global management standards and technological It comprises detailed datasheets that initiative on invasive species led by the translations to ensure that retrieval and have been sourced from experts, edited Global Invasive Species Programme exchange of information can take place by CABI's scientific staff, peer-reviewed, (GISP) and is supported through across political, linguistic, technological, enhanced with data from specialist partnerships with the National Biological and institutional boundaries. organisations, and with images, and Information Infrastructure, Manaaki maps, and linked to a bibliographic Whenua-Landcare Research, the Critical www.gisin.org database. Ecosystem Partnership Fund, the University of Auckland and private Content is derived from thousands of donations. The Programme of Work on Invasive peer-reviewed expert contributors, Alien Species of the Convention on backed up by existing compilations of The Global Invasive Species Database Biological Diversity knowledge and research on invasive focuses on invasive alien species that species. It offers extensive global threaten native biodiversity and covers The Conference of the Parties (COP) to coverage of all invasive species, from all taxonomic groups from micro- the Convention on Biological Diversity every taxonomic group (excluding organisms to animals and plants in all (CBD) has recognized that there is an human pathogens), with fast and easy ecosystems. Species information is urgent need to address the impact of navigation between text, images, maps either supplied by or reviewed by expert invasive alien species (IAS), and has and databases. contributors from around the world. established IAS as a cross-cutting issue. A portal on the CBD website has been The compendium is a vital tool for www.issg.org/database designed as a gateway to information resource managers, extension workers, relating to invasive alien species. policymakers and researchers in the areas of agriculture and the environment. The Global Invasive Species www.cbd.int/invasive/ It will be freely available to all on an open Information Network access basis and will be maintained, enhanced and regularly updated into the The GISIN is a Web-based network of future, on a sustainable basis. data providers including government, non-government, non-profit, educational, The ISC is a constantly developing and other organizations that agree to work encyclopaedic resource containing: together to provide increased access to Please register your contributions to the International Agenda for Botanic Gardens in Conservation

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