Carol A. Ellison

Prospects for the Management of Invasive Alien Weeds Using Co-Evolved Fungal Pathogens: A Latin American Perspective

Invasive alien weeds pose a serious threat to the biodiversity of natural ecosystems and a significant constraint to agricultural production worldwide. The use of co-evolved natural enemies, a strategy referred to as classical biological control (CBC), has proven to be a potentially efficacious, cost-effective, and safe option for the management of alien weeds. An analysis of CBC of invasive weeds in Latin America is presented, which shows that only 5% of the worldwide releases of agents, overwhelmingly arthropod, have been in this region. Fungal pathogens are increasingly being considered in CBC programmes, and there are now 11 examples of Latin American fungi having been released as biocontrol agents in other regions of the world. In contrast, only three weed pathogens have been deliberately released in the region. Possible reasons for the paucity of CBC programmes in Latin America are presented, despite the presence of a significant number of alien weed species (60 are listed). An analysis of these weeds reveals that many of them could be amenable to control using natural enemies, including nine weed species for which CBC programmes have been successfully implemented elsewhere in the world. In addition, for many of these 60 species, a co-evolved and damaging mycobiota has already been recorded. The prospects for management of invasive alien weeds in Latin America, using co-evolved fungal pathogens, are assessed with particular reference to selected species from the genera Ambrosia, Broussonetia, Calotropis, Commelina, Cyperus, Dichrostachys, Echinochloa, Pittosporum, Rottboellia, Rubus, Sonchus and Ulex.

Integrating mitigation and adaptation into development: the case of Jatropha curcas in sub-Saharan Africa

BART MUYS , L INDSEY NORGROVE , TENA ALAMIREW , RHODA B IRECH , EL I SA CH IR IN IAN , YOSEPH DELELEGN , ALBRECHT EHRENSPERGER , CAROL A . ELL I SON , ADEM FETO , BERNHARD FREYER , JAN GEVAERT , S IMON GM € UNDER , RAYMOND E . E . JONGSCHAAP , MANFRED KAUFMANN , JOD IE KEANE , MARC KEN I S , BON I FACE K ITEME , JACKSON LANGAT , REG INALD LY IMO , V IOLET MORAA , JAC INTA MUCHUGU , AKL I LU NEGUSS I E , CAROL INE OUKO , MATHUR IN W . ROUAMBA , I R IA SOTO , MANFRED W € ORGETTER , RA INER ZAH and RIGOBERTO ZETINA

Studies on the rust Prospodium tuberculatum, a new classical biological control agent released against the invasive alien weed Lantana camara in Australia. 1. Life-cycle and infection parameters.

The neotropical rust fungus Prospodium tuberculatum was released in Australia in 2001 for the classical biological control of the invasive alienweed Lantana camara, following a risk assessment that included studies on its life-cycle, infection parameters and host range. This paper reports on the first two research areas. This rust is recorded as autoecious and microcyclic (urediniospores and teliospores only) in the literature, but the role of the teliospores had not been demonstrated. Extensive field surveys reported here found the rust to cycle solely through urediniospores on L. camara throughout most of its native range. However, at the high altitude extremes of its range, the rust has retained its ability to over-winter as teliospores. Attempts to clarify the function of the basidiospores and the conditions necessary to induce teliospore formation were unsuccessful under controlled conditions. A hypothesised connection between P. tuberculatum and Aecidium lantanae was rejected after DNAanalysis. Investigations on spore storage showed that teliospores and urediniospores can survive for extended periods in liquid nitrogen. Glasshousebased studies demonstrated that the urediniospores have wide temperature tolerance (10–25°C) for infection of L. camara, with an optimum near to 20°C. The minimum dew period requirement for plant infection was 9 h with the optimum close to 15 h.

Studies on the rust Prospodium tuberculatum, a new classical biological control agent released against the invasive alien weed Lantana camara in Australia. 2. Host range

A strain of the rust Prospodium tuberculatum from Brazil was screened as a potential biocontrol agent against 40 Australian Lantana camara forms and 52 closely related, non-target plant species. Results under glasshouse conditions showed that the Brazilian rust strain is pathogenic to only two flower colour forms: pink and pink-edged red. Macro- and microsymptoms were recorded using 11 assessment categories and four susceptibility ratings. No macrosymptoms were observed on any of the non-target plants. Additional keywords: fungus, pathogens.

Puccinia komarovii var. glanduliferae var. nov.: a fungal agent for the biological control of Himalayan balsam (Impatiens glandulifera)

Clearly defining the taxonomic identity of a potential biocontrol agent is an essential component of any biological control programme. As part of such a programme against Impatiens glandulifera, a highly invasive annual weed in both Europe and North America, the rust fungus Puccinia komarovii was collected on this host plant in its native Himalayan range. However, current literature indicates that P. komarovii is a pathogen of a number of Impatiens species globally and was described originally from I. parviflora, a species native to Asia and now naturalized in Europe. Morphological comparisons, based on urediniospore and teliospore measurements, were generally inconclusive in showing any clear differences between the accession from I. glandulifera and those from other Impatiens species. Both, nrDNA ITS and ITS2-LSU sequence analyses indicated a difference between the rust infecting I. glandulifera compared to accessions on other hosts. However, the large variations in both ITS and 28S (ITS2-LSU) sequences determined within single accessions in this study, makes a clear separation difficult. Cross-inoculation experiments, using one accession of P. komarovii ex I. glandulifera (from India) and two accessions of P. komarovii ex I. parviflora (from China and Hungary), confirmed the specificity of these strains to their original hosts. Two Himalayan Impatiens species, I. scabrida and I. brachycentra, showed varying levels of susceptibility to these rust accessions, where the former was weakly susceptible to all three accessions and the latter was weakly susceptible only to P. komarovii ex I. parviflora (from China). However, commercial cultivars of I. balsamina proved to be fully susceptible to all rust accessions, although this has not been demonstrated under field conditions in India. Based on these host specificity differences between the rust accessions, we propose a new variety: Puccinia komarovii var. glanduliferae var. nov. associated with I. glandulifera in the Himalayas.

Weed biological control in the European Union: from serendipity to strategy

Biological control of weeds is a globally recognised approach to the management of some of the most troublesome invasive plants in the world. Accidental introductions of agents accounted for all weed biological control agent establishments in the European Union until 2010, but these examples include some current or emerging control successes both large and small, from the redistribution of the weevil Stenopelmus rufinasus Gyllenhal (Coleoptera: Curculionidae) for the control of small outbreaks of Azolla filiculoides Lam. (Azollaceae), to the large scale control provided by the cochineal insect Dactylopius opuntiae (Cockerell) (Hemiptera: Dactylopiidae), used against some problematic prickly pears (Opuntia spp. (Cactaceae)), and the ragweed beetle Ophraella communa LeSage (Coleoptera: Chrysomelidae), against common ragweed, Ambrosia artemisiifolia L. (Asteraceae), which are providing benefits to an increasing number of Member States of the European Union. Recent programmes involving the intentional introduction of biological control agents against target weeds including Fallopia japonica (Hout.) Ronse Decr. (Polygonaceae), Impatiens glandulifera Royle (Balsaminaceae) and Acacia longifolia (Andrews) Willd (Fabaceae) show a shift from luck to judgement in the European Union. The inclusion of new weed targets on the European Invasive Species Regulation should lead to a growth in the profile and use of biological control which would be assisted by the publication of any successes from the few intentional introductions covered in this paper.

Community consequences of introducing a biological control agent, NERC

In the UK, and much of Europe and the rest of the world, invasive weeds are destroying natural habitats through exclusion of native species, reduction of biodiversity, and removal of ecosystem services. Some invasive weeds even damage the groundwork of buildings, causing structural problems. The costs to the UK economy alone totals almost £2billion per year highlighting them as key targets for control or removal. Efforts to control these weeds is also problematic and expensive, partly due to lack of control measures and partly because of the vigorous nature of the plant spread and deep-rooted establishment of the plants. One of these problem plants is Impatiens glandulifera (Himalayan Balsam), which is now the most commonly occurring non-native plant species on riparian (riverside) systems in England and Wales. The plant severely reduces native plant and insect biodiversity and is expensive and difficult to control, because herbicides cannot be used near water courses. Balsam plants die off in winter, leaving exposed areas susceptible to erosion, while summer populations choke water courses, increasing the likelihood of flooding. DEFRA selected Balsam as target weed for biological control, emphasising the importance of this research. In July 2014, CABI received Ministerial approval to release the rust fungus Puccinia komarovii var. glanduliferae, a pathogen of Himalayan Balsam found in Pakistan and India, at trial sites in the UK. This is the first approved release of a non-native fungal pathogen anywhere in Europe. It therefore provides a unique opportunity to determine the impact of the rust release on the plant and the communities it has invaded. It is important not just to examine what factors affect the efficacy of the rust in the field, but also how native plant communities recover as weed populations decline. This proposal is a joint one involving CABI, Royal Holloway, University of London and the University of Reading. Together, we will monitor rust release, determine the factors that affect its establishment in the field and discover how invaded communities recover after balsam removal. We will conduct this research alongside DEFRA, who have pledged money to monitor rust release. We will carry out a series of experiments to examine the impact of soil-dwelling beneficial fungi (termed arbuscular mycorrhizas) on rust infection. Mycorrhizas provide plants with essential nutrients and some species are known to increase susceptibility to foliar pathogens. We will also examine the foliar tissues of balsam plants, as these also contain fungi (termed endophytes). New research is emerging to suggest that microbes living on plant surfaces and inside plants could have anti-microbial effects on potential invading pathogens. It is critical to determine whether we can manipulate the plants growth conditions to maximise the efficiency of the rust, either through encouraging microbes that help the rust or removing conditions for detrimental microbes. This is a unique opportunity to discover how the native plant, insect and soil microbial communities start to recover after weed removal. Biocontrol is usually about reducing the health or performance of target organisms and to date it has generally been assumed that a native, diverse community will readily establish. However, we know that balsam somehow alters the soil to severely reduce growth of other plants. Thus, a key outcome of the study will be to determine how we can use beneficial microbes to allow native plants to recolonise. A particularly exciting part is that the mycorrhizal fungi which we hope to use to aid rust efficacy also have the potential to help native plants to grow, thus we will be able to develop a unique, double-headed strategy to have a genuine impact on the control of this weed.

Erratum: Puccinia komarovii var. glanduliferae var. nov.: a fungal agent for the biological control of Himalayan balsam (Impatiens glandulifera) [Eur J Plant Pathol, DOI 10.1007/s10658-014-0539-x]

Clearly defining the taxonomic identity of a potential biocontrol agent is an essential component of any biological control programme. As part of such a programme against Impatiens glandulifera, a highly invasive annual weed in both Europe and North America, the rust fungus Puccinia komaroviiwas collected on this host plant in its native Himalayan range. However, current literature indicates that P. komarovii is a pathogen of a number of Impatiens species globally and was described originally from I. parviflora, a species native to Asia and now naturalized in Europe. Morphological comparisons, based on urediniospore and teliospore measurements, were generally inconclusive in showing any clear differences between the accession from I. glandulifera and those from other Impatiens species. Both, nrDNA ITS and ITS2-LSU sequence analyses indicated a difference between the rust infecting I. glandulifera compared to accessions on other hosts. However, the large variations in both ITS and 28S (ITS2-LSU) sequences determined within single accessions in this study, makes a clear separation difficult. Cross-inoculation experiments, using one accession of P. komarovii ex I. glandulifera (from India) and two accessions of P. komarovii ex I. parviflora (from China and Hungary), confirmed the specificity of these strains to their original hosts. Two Himalayan Impatiens species, Eur J Plant Pathol (2015) 141:247–266 DOI 10.1007/s10658-014-0539-x R. A. Tanner (*) : C. A. Ellison :M. K. Seier : S. Varia : D. Djeddour :H. C. Evans CABI, Bakeham Lane, Egham, Surrey TW20 9TY, UK e-mail: r.tanner@cabi.org G. M. Kovács : E. Kassai-Jáger : Z. Berecky : L. Kiss (*) Plant Protection Institute, Centre for Agricultural Research, Hungarian Academy of Sciences (MTA), 1525 Budapest, P.O. Box 102, Hungary e-mail: kiss.levente@agrar.mta.hu G. M. Kovács Institute of Biology, Department of Plant Anatomy, Eötvös Loránd University, 1117 Pázmány Péter sétány 1/C, Budapest, Hungary E. Kassai-Jáger Faculty of Health Sciences, Institute of Health Promotion and Clinical Methodology, Department of Epidemiology, Semmelweis University, 1085 Üllői út 26, Budapest, Hungary M. C. Singh National Bureau of Plant Genetic Resources, Pusa Campus, New Delhi, India Á. Csiszár Department of Botany and Nature Conservation, Faculty of Forestry, University of West Hungary, Sopron, Hungary P. Csontos Institute for Soil Science and Agricultural Chemistry, Centre for Agricultural Research, Hungarian Academy of Sciences (MTA), Budapest, Hungary I. scabrida and I. brachycentra, showed varying levels of susceptibility to these rust accessions, where the former was weakly susceptible to all three accessions and the latter was weakly susceptible only to P. komarovii ex I. parviflora (from China). However, commercial cultivars of I. balsamina proved to be fully susceptible to all rust accessions, although this has not been demonstrated under field conditions in India. Based on these host specificity differences between the rust accessions, we propose a new variety: Puccinia komarovii var. glanduliferae var. nov. associated with I. glandulifera in the Himalayas.