Introductions of non-native plant pathogens into Great Britain, 1970–2004

Authors


*E-mail: bananadoctor@msn.com

Abstract

An analysis of records of plant pathogens first identified in Great Britain from 1970 to 2004 (inclusive) was undertaken to determine the numbers of new species that have become established over time. Results show that the numbers of newly recorded pathogens have not varied significantly. Of the 234 pathogens recorded for the first time between 1970 and 2004, 157 were fungi, 27 were oomycetes, 26 were viruses, 23 were bacteria, and one was a phytoplasma. Approximately 53% of pathogens were found on ornamental crops, 16% on horticultural crops, 15% on wild native species, 12% on agricultural crops, 2% on pasture plants and 2% on exotic forestry tree species. Where the origin of introductions was known or strongly suspected, 47% came from the Netherlands. About 38% of newly recorded pathogens with information on the location of first record were discovered in the South East region of England. Plant Pathologists regarded 19% of all new pathogens as important because of actual or potential economic/environmental losses. The results indicate that the numbers of new or important pathogens establishing in recent years are not increasing and that most new findings are associated with ornamental plants.

Introduction

The risks posed by the importation of plants that harbour non-native pathogens are well known (Wilson & Graham, 1983; Ebbels, 2003) and have recently been highlighted (Brasier, 2005; Henricot & Gorton, 2005; Ingram, 2005; Webber & Brasier, 2005). More effective intelligence to identify risks early and a self-regulated limitation of imports by the nursery plant trade have been suggested as means of preventing the entry and establishment of non-native organisms that could damage crops and ecosystems (Brasier, 2005).

Comprehensive check lists of plant pathogens and their hosts have been published for a number of countries (e.g. Conners, 1967; Pennycook, 1989; Singh, 1980) and even for political divisions within large countries (e.g. Alfieri et al., 1984; Cook & Dubé, 1989), from time to time. Some check lists only cover one group of organisms, of which some are pathogens (e.g. Farr et al., 1989), or one type of pathogen within a group, e.g. the rust fungi, (Henderson, 2000).

Check lists summarizing all pathogens present in a country are fundamental to plant health and quarantine legislation (Shivas et al., 2006). Check lists often do not include the year of entry or first record of a pathogen, its first recorded host and pathway of introduction. However, these data are essential for trends in plant pathogen incursions to be determined.

Little work has been undertaken on calculating the numbers and types of non-native plant pathogens and pests introduced into Great Britain. Some check lists have been compiled (Moore, 1959) and information on common diseases collated (Baker, 1972). Some new records have been published either as a regular item or on an ad hoc basis in scientific journals, or included in books and booklets (e.g. Preece, 2002). Other lists have been maintained independently by organizations, such as the Central Science Laboratory (CSL) of the Department for Environment, Food and Rural Affairs (Defra) and also the British Mycological Society. However, no one body has been responsible for keeping a comprehensive list of all pathogens for Great Britain. This has caused difficulties in the compilation of a comprehensive list of pathogen introductions for the period 1970 to 2004.

An analysis has recently been undertaken of invertebrate plant pest introduction into Great Britain (Smith et al., 2005) and English Nature has compiled an audit of non-native species, which includes some important plant pathogens (Hill et al., 2005). However, there has been no attempt to produce a host–pathogen database for all groups of pathogens containing the information required to identify any significant trends that would be of use to the plant health authorities.

This paper is an attempt to list all new plant pathogens introduced into Great Britain from 1970 to 2004 (inclusive), though, given the scattered distribution of this information in various publications and official documents, it is almost certain the list is not fully comprehensive. Indeed, it is likely that a few entries will be first records of established pathogens. Other pathogens may have been recorded once on an imported plant in a glasshouse and then died out. A reference to the first record has been given to each entry. If information was available from the literature and government records, the pathogen's origin, pathway of entry and location of where first discovered were also recorded.

The work reported here was undertaken in order to determine as accurately as possible the number of pathogen introductions, the types of pathogens introduced, the infected hosts imported, the means of introduction, countries of origin and the significance of the introductions. The data were analysed to determine whether it is possible to detect trends in the invasion of non-native pathogens, the types of pathogens likely to gain entry and countries from which importations pose a higher risk. This is the first analysis of its kind undertaken in Great Britain.

Methods

Information on plant pathogenic fungi and oomycetes was obtained from archived files, indices and lists compiled by mycologists at the CSL in the course of their duties diagnosing plant disease specimens. These specimens were sent for identification by the Plant Health and Seeds Inspectorate (PHSI), which is responsible for inspecting plant imports and certain crops in England and Wales, staff of ADAS (formerly the Agricultural Development and Advisory Service before privatization), which has advisory scientists in the field, and the public, who submit material from nurseries or gardens. New records published in the scientific literature, such as in Plant Pathology [http://www.blackwellpublishing.com/ppa] and Mycologist [http://www.elsevier.com/locatew/mycol], have been another source. More obscure entries were cross-checked with the list of British fungal pathogens provided online by the British Mycological Society in their Fungal Records Database (BMSFRD) (Anonymous, 2005c) if the year or place of the first record was in doubt. Sometimes, the BMSFRD entry was more citable than the original reference, but the BMSFRD was not used as a primary source of information. Mycologists at CSL and Forest Research Agency, Alice Holt Lodge, Farnham, GU10 4LH, UK also gave advice and information. Synonyms and taxonomic re-evaluations have been accommodated, but some names may still not reflect the latest taxonomic viewpoints. For rust pathogens, advice given by Henderson (2000) was followed. Where a species present in Great Britain before 1970 has been split into numerous new species, such as has happened to the smut Microbotryum violaceum (Spooner & Legon, 2006), the new species have not been included in this analysis.

Information on the new bacterial, phytoplasma and virus pathogens, which have been recorded in Great Britain from 1970 to 2004, and advice on their importance was provided by CSL specialists, who consulted their personal lists and also records in the National Collection of Plant Pathogenic Bacteria (Anonymous, 2003). These specialists also diagnose disease specimens for PHSI, ADAS and the public, and have information on new disease outbreaks. Information has also come from the scientific literature. Those new viruses that have not been described or named, such as a tobravirus found in ash (Fraxinus excelsior) (Cooper et al., 1983) and a tobamovirus detected in rose (Rosa sp.) (Hicks & Frost, 1984), have not been taken into consideration. Some papers written after 1970 describe viruses introduced in plants prior to 1970 (e.g. Jones, 1972). Viruses found in the weed genus Plantago (Hammond, 1981) are almost certainly of local origin and have also been omitted.

In this document, ‘introduction’ is defined as both ‘entry’ and ‘establishment’. Pathogens that were regarded as present in Great Britain, but which were subject to official eradication measures on 31 December 2004, have been included. Pathogens that are known to have entered, but did not establish because of eradication or natural disappearance before 31 December 2004, have been omitted. This includes pathogens that were intercepted on imported plants and produce. Most intercepted pathogens did not establish because the host or consignment was destroyed at the point of detection. An example of an important pathogen that entered, but was eradicated before establishment is Chrysanthemum stem necrosis virus (CSNV). This virus was found in a nursery that had imported infected chrysanthemum (Chrysanthemum ×morifolium) cuttings from Brazil (Mumford et al., 2003), but was eradicated before the end of 2004 after an extensive campaign that included the destruction of infected plants and the control of Frankliniella occidentalis, the thrips vector present in the glasshouse (Matthews et al., 2005). Another example is ‘Candidatus Phytoplasma mali’, the cause of apple proliferation disease, which was found once in one apple tree (Malus pumila) in Essex, SE England in 1978 (Davies et al., 1986). This tree was destroyed after the disease was confirmed and no further cases have been reported. The origin of the phytoplasma could not be determined because the orchard was established from local stocks. The fungus Fusarium foetens, the cause of a serious crown rot of ornamental Begonia × hiemalis cv. Elatior, which was imported from the Netherlands in 2002, is another pathogen that is no longer found in Great Britain and is now officially regarded as eradicated (P. Reed, CSL, personal communication).

Some minor pathogens that were detected on imported material by PHSI may not have been eradicated, because they were considered too unimportant to merit statutory control. In these cases, advice usually given by PHSI to the importer is that destruction of the infected plant, although not obligatory, would be prudent. However, no guarantee can be given that this advice was heeded. Since establishment may have occurred, these pathogens have been included on the list. However, in some cases, the first diagnosis may have been the only record.

In a few instances, pathogens recorded for the first time after 1970 seem highly likely to have gained entry prior to 1970. An example is Ophiostoma novo-ulmi subsp. americana (Brasier & Kirk, 2001), the cause of a more severe form of Dutch elm disease, which already existed in Great Britain. It was first recognized in 1971 (Gibbs & Brasier, 1973), but is likely to have been introduced in the late 1960s. It is speculated that timber imported from the USA was the source (Anonymous, 2005d), but this cannot be proven. As the pathogen is considered to have entered Great Britain prior to 1970, it has not been included in this analysis.

The paper contains new introduction records up until the end of 2004. Those pathogens identified in 2005/2006 and whose presence in 2004 cannot be proven have not been included. Examples in this category are the seedborne bacteria Xanthomonas hortorum pv. carotae and X. campestris pv. zinniae.

Unlike many well known groups of organisms, there is no British list for plant pathogens and it is therefore difficult to be certain of their non-native status. For example, Pythium tracheiphilum, was described as pathogenic on lettuce (Lactuca sativa) in 1988, although it was first isolated from soil in Great Britain in 1981, and, as such, could be a common soil inhabitant that has been present prior to 1970. Such species have been included in this survey. However, where there is documented evidence that the pathogen entered the country prior to 1970, the pathogen has not been included in the list.

Some pathogens detected in one nursery are known or suspected to have become established because of an undetected entry through another nursery. Calibrachoa mottle virus falls in this category. Although quarantine action was taken when the virus was first found in the ornamental Calibrachoa (‘Million Bells’ series) from the Netherlands, the virus was subsequently found to be widespread in imported plants. Following the discovery of the virus, the industry has ensured that Calibrachoa stocks used for propagation are virus-free (R. Mumford, CSL, personal communication).

Isolates of a different mating type to one already introduced, such as the oomycete Phytophthora infestans A2 mating type, have also been included. Strains of other types of pathogens introduced between 1970 and 2004 that have been shown to be different from strains already present have also been included e.g. the resistance breaking strain of Raspberry bushy dwarf virus (RBDV).

Pathogens infecting edible mushroom (Agaricus bisporus), such as the bacterium Burkholderia gladioli pv. agricola first recorded in 1987, have not been included as this review is restricted to pathogens of plants.

Those introduced pathogens that have been recorded as seedborne by Richardson (1990) or other sources have been identified on Table 1. Some, such as Fusarium oxysporum f. sp. basilici, have been linked to seed imports.

Table 1.  Plant pathogens introduced into Great Britain from 1970 to 2004
PathogenDiseaseHostYearPathwayOriginLocation of first recordReference(s)
  1. Key: Pathogen name: 1 = reported as seed-borne by Richardson (1990) or other sources; * = important pathogen; † = entered Great Britain before 31·12, 04 – under eradication on 31·8·06.

  2. Host type: A = agricultural crop; H = horticultural crop; N = wild plant or tree native to the UK; O = ornamental plant or tree; P = pasture plant; T = forestry tree.

  3. Pathway: IH = imported host including plant, seedling, cutting, tuber, etc.; IS = imported seed; NIC = no direct import connection.

  4. Origin: CI = Cote d’Ivoire; CY = Cyprus; E = Europe; FR = France; IN = India; IT = Italy; NL = the Netherlands; NZ = New Zealand; US = United States of America.

  5. References: ADAS = Agricultural Development and Advisory Service; CSL = Central Science Laboratory; MAFF = Ministry of Agriculture, Fisheries and Food; SCRI = Scottish Crop Research Institute.

  6. Virus names: names in italics are recognised species; names in roman are tentative species.

Fungi
Alternaria dennisiiLeaf spot of ragwortSenecio jacobaeaN1970NIC Isle of ManEllis (1971) pp. 27–28.
Alternaria petroselini1Leaf blotch of parsleyPetroselinum crispumH1975NIC WorcestershireEllis (1976) p. 417
Anthostomella conorumInfection of cone scales of Corsican pinePinus nigra subsp. laricioT1976NIC ScotlandFrancis (1978)
Anthostomella formosa Infection of needles of Corsican pinePinus nigra subsp. laricioT1971NIC ScotlandFrancis (1978)
Anthostomella pedemontanaInfection of needles of Scots pinePinus sylvestrisN1975NIC ScotlandFrancis (1978)
Anthostomella sabinianaeInfection of needles of Corsican pinePinus nigra subsp. laricioT1976NIC ScotlandFrancis (1978)
Ascochyta allii-cepaeLeaf spot of onionAllium cepaA1982NIC SuffolkCentral Science Laboratory records
Ascochyta ampelinaDieback of Virginia creeperParthenocissus ampelinaO1973IHNLWorcestershireMAFF, Harpenden – internal document
Ascochyta elaeagniLeaf spot of elaeagnusElaeagnus ×ebbingeiO1985NIC HampshireCentral Science Laboratory records
Ascochyta imperfecta1Leaf spot of lucerneMedicago sativaP1978NIC  Central Science Laboratory records
Ascochyta infuscansLeaf spot of pasque flowerPulsatilla vulgarisO1982NIC NorfolkCentral Science Laboratory records
Ascochyta lobikii Leaf spot of onionAllium cepaA1982NIC CambridgeshireCentral Science Laboratory records
Ascochyta suberosaLeaf spot of lettuceLactuca sativaH1976NIC West SussexCentral Science Laboratory records
Bauerago vuyckiiLeaf smut of field wood-rushLuzula campestrisN1998NIC WarwickshireSmeathers (1998)
Ceratocystis laricicolaWilt/root rot of larchLarix deciduaT1972NIC ScotlandRedfern et al. (1987)
Ceratocystis radicicolaWilt/root rot of pinePinus sp.T1976NIC  Ellis (1976) p. 37
Cercoseptoria moravicaLeaf spot of kingcupCaltha palustrisN1982NIC DorsetCentral Science Laboratory records
Cercospora armoraciaeLeaf spot of horse-radishArmoracia rusticanaH1976NIC  Ellis (1976) p. 254
Cercospora bidentisLeaf spot of bur-marigoldBidens sp.N1976NIC  Ellis (1976) p. 250
Cercospora chenopodiiLeaf spot of chenopodiumChenopodium sp.N1976NIC  Ellis (1976) pp. 248–9
Cercospora crepidisLeaf spot of smooth hawk's beardCrepis capillarisN2000NIC SurreySpooner (2002)
Cercospora juncicolaLeaf spot of salt rushJuncus effususN1976NIC  Ellis (1976) p. 262
Cercospora loti1Leaf spot of birds foot trefoilLotus corniculatusN1976NIC  Ellis (1976) p. 267
Cercospora moellerianaLeaf spot of strawberry treeArbutus unedoO1994IH  Central Science Laboratory records
Cercospora nigellaeLeaf and capsule spot of devil-in-a-bushNigella sp.O1976NIC  Ellis (1976) p. 280
Cercospora radiataLeaf spot of anthyllisAnthyllis sp.N1976NIC  Ellis (1976) p. 265
Ciborinia camelliae*Petal blight of camelliaCamellia japonicaO1999NIC DevonCook (1999)
Cladosporium magnusianumLeaf tip blight of bog aspinelNarthecium ossifragumN1976NIC  Ellis (1976) pp. 337–338
Cladosporium orchidisLeaf spot of fen orchidDactylorhiza praetermissaN 1976NIC NorfolkEllis (1976) p. 338
Clasterosporium flexumTwig rot of Lawson's cypressChamaecyparis lawsonianaO1981NIC ScotlandSutton et al. (1994); British Mycological Society Fungal Records Database
Cochliobolus carbonum1Leaf spot of maizeZea maysA1972ISFRLincolnshireCentral Science Laboratory records; Ellis & Holiday (1972)
Coleroa alchemillaeLeaf spot of lady's mantleAlchemilla vulgarisO1978NIC  Dennis (1978) p. 377
Colletotrichum acutatumLeaf curl/corm rot of anemoneAnemone sp.O1978NIC JerseyMAFF Plant Pathologist's Quarterly Record 1978 No.4 p.15
Coniothyrium fragariae Crown necrosis of strawberryFragaria × ananassaH1972NIC ScotlandJarvis & Hargreaves (1972)
Coniothyrium lavandulae*Dieback of lavenderLavandula angustifoliaO1979NIC NorfolkHumphreys-Jones (1981)
Curvularia trifolii f. sp. gladioli1Leaf spot of gladioliGladiolus sp.O1985IHUSIsle of WightCentral Science Laboratory records
Cylindrocladiella camelliaeStem and root rot of pelargoniumPelargonium sp.O1991IHNLCumbriaCentral Science Laboratory records
Cylindrocladiella parva*Stem rot of pelargoniumPelargonium sp.O1980NIC  MAFF East Midlands – internal document
Cylindrocladium buxicola*Box blightBuxus microphyllaO1994NIC HampshireSellar (1995)
Cylindrocladium ilicicolaLeaf spot of bayLaurus nobilisO1985NIC Isles of ScillyBrayford & Chapman (1987)
Cylindrocladium pauciramosumStem lesions of ceanothusCeanothus sp.O2002NIC East AngliaLane et al. (2006)
Cylindrocladium spathiphylliLeaf and root rot of spathiphyllumSpathiphyllum sp.O1991IHNLLincolnshireCentral Science Laboratory records
Dichotomophthora portulacae1Leaf spot of purslanePortulaca oleraceaO1982ISCYHertfordshireCentral Science Laboratory records
Didymella ligulicola var. inoxydabilisStem rot of pyrethrumTanacetum coccineumO2001NIC  MAFF Plant Pathologist's Quarterly Report 2001 Jan–Mar
Dietelia codiaeiRust of crotonCodiaeum variegatumO1978IHCI Boerema et al. (1994)
Discula destructiva*Anthracnose of dogwoodCornus floridaO1993NICUSYorkshireSellar (1995); Tuffs (1995)
Elsinoe mattiroloanumLeaf spot of strawberry treeArbutus unedoO1978NIC  ADAS, Cambridge
Entyloma crepidis-rubraeLeaf smut of smooth hawk's beardCrepis capillarisN2000NIC SurreySpooner (2000)
Entyloma ellisiiLeaf smut of spinachSpinacia oleraceaeA1990NIC WarwickshireHorticultural Research Institute, Wellesbourne, UK
Entyloma veronicaeLeaf smut of thyme-leaved speedwellVeronica serpyllifoliaN1997NIC SurreyPegler et al. (1999)
Erysiphe astragaliPowdery mildew of milk-vetchAstragalus glycyphyllosN1975NIC  Tapster & Bailey (1975)
Erysiphe australianaPowdery mildew of crape-myrtleLagerstroemia indicaO1972NIC HampshireCentral Science Laboratory records
Erysiphe azaleae*Powdery mildew of rhododendronRhododendron sp.O1980NIC SurreyCentral Science Laboratory records; Ing (2000)
Erysiphe biocellataPowdery mildew of bugleAjuga genevensisO1990NIC  Ing (1990a)
Erysiphe brunneopunctataPowdery mildew of monkey flowerMimulus guttatusO1990NIC  Ing (1990a)
Erysiphe catalpaePowdery mildew of Indian bean tree (1)Catalpa bignonioidesO1990NIC  Ing (1990a,c)
Erysiphe diffusaPowdery mildew of sophoraSophora flavescensO1991NIC  Ing (1991)
Erysiphe elevataPowdery mildew of Indian bean tree (2)Catalpa bignonioidesO 2004NICUSSurreyCook et al. (2004)
Erysiphe flexuosaPowdery mildew of horse chestnutAesculus × carneaO2002NIC  Ing & Spooner (2002)
Erysiphe guarinoniPowdery mildew of laburnumLaburnum anagyroidesO1990NIC  Ing (1990d)
Erysiphe howeanaPowdery mildew of evening primroseOenothera biennisO1988NIC  O’Neill et al. (1991)
Erysiphe mayoriiPowdery mildew of thistleCirsium arvensisN 1991NIC  Ing (1990a,c)
Erysiphe palczewskiiPowdery mildew of pea treeCaragana arborescensO1999NIC SurreySpooner (2001b)
Erysiphe plataniPowdery mildew of plane treePlatanus×acerifoliaO 1983NIC  Central Science Laboratory records
Erysiphe rayssiaePowdery mildew of Spanish broomSpartium junceumO1975NIC  Tapster & Bailey (1975)
Erysiphe russelliiPowdery mildew of yellow sorrelOxalis corniculataO1975NIC  Tapster & Bailey (1975)
Erysiphe sp.Powdery mildew of white heatherCalluna vulgarisO2000NIC ScotlandMcQuilken et al. (2002)
Erysiphe symphoricarpiPowdery mildew of snowberrySymphoricarpos albusO1990NIC LeicestershireKiss et al. (2002)
Erysiphe syringaePowdery mildew of ligustrumLigustrum ovalifoliumO1990NIC  Ing (1990d)
Erysiphe thermopsidisPowdery mildew of thermopsisThermopsis lanceolataO1991NIC  Ing (1991)
Fusarium langethiaeFusarium head blight of wheatTriticum aestivumA1998NIC  Wilson et al. (2004)
Fusarium lateritium var. buxiCanker of boxBuxus sp.O1971NIC  Monthly Summary 1971
Fusarium oxysporum f. sp. basiliciWilt of basilOcimum basilicumH1997ISIT Central Science Laboratory – diagnosis of ADAS sample
Fusarium oxysporum f. sp. radicis-lycopersici*Fusarium crown rot of tomatoLycopersicon esculentumH1983IHNLSouth East EnglandThe Grower 17 March 1988
Fusarium trichothecioides*Dry rot/gangrene of potatoSolanum tuberosumA1982IHNL Sellar (1982)
Gliocladium vermoeseniiStem rot of areca nut palmAreca sp.O1991NIC YorkshireADAS Leeds
Glomerella cingulata f. sp. camelliae1Dieback/leaf blotch of camelliaCamellia saluenensis hybridsO1982IHNZHampshireCentral Science Laboratory records; Dickens & Cook (1989)
Golovinomyces cynoglossiPowdery mildew of borageBorago officinalisO1988NIC EssexO’Neill et al. (1991)
Golovinomyces echinopsisPowdery mildew of globethistleEchinops bannaticusO1990NIC  Ing (1990c)
Golovinomyces magnicellulataPowdery mildew of phloxPhlox drummondiiO1990NIC  Ing (1990d) as Erysiphe magnicellulatus
Insolibasidium deformans Leaf blight of honeysuckleLonicera nitidaO2000NIC South East EnglandBeales et al. (2004)
Kabatiella zeae*1Eyespot of maizeZea maysA1998ISESouth West EnglandSansford & Cooper (1998)
Kabatina thujaeShoot base canker of Lawson's cypressChamaecyparis lawsonianaO1976IS ScotlandMAFF Plant Pathologist's Quarterly Record 1976, p. 30
Kirramyces phormi Leaf spot of phormiumPhormium colensoiO1983IHNZ Central Science Laboratory records
Lambertella corni-marisFruit rot of appleMalus domesticaH1992NIC  ADAS Plant Clinic, Cambridge
Macrophoma japonicaLeaf spot on sun-scorched leafCamellia japonicaO1986NIC DorsetCentral Science Laboratory records
Mamianiella coryliLeaf spot of hazelnutCorylus sp.H1978NIC  Dennis (1978), p. 361
Melanopsichum nepalenseFlower axis smut of knotweedPolygonum aviculareN1984NIC SurreySpooner (1985)
Microdiplodia ceanothiWilt/stem rot of ceanothusCeanothus dentatusO1979NIC NorfolkCentral Science Laboratory records
Microsphaeropsis pittospororumLeaf spot of pittosporumPittosporum ‘Garnetti’O1982IHNZDevonCentral Science Laboratory records
Mikronegeria fagiRust of southern beechNothofagus sp.O1976NIC GloucestershireBritish Mycological Society Fungal Records Database
Milesia magnusianaRust of black spleenwortAsplenium adiantum-nigrumN1970NIC South West EnglandHenderson (2000)
Mycosphaerella linicola1Pasmo disease of linseedLinum usitatissimumA1975ISEScotlandCentral Science Laboratory records; Holmes (1976)
Mycosphaerella mollerianaShoot dieback of gumEucalyptus gunniiO1986NIC SurreyCentral Science Laboratory records
Neoerysiphe galeopsidisPowdery mildew of catalpaCatalpa spp.O2004NIC  Henricot & Cook (2005)
Oidium acrocladumPowdery mildew of stepeliaStapelia hanburyanaO1973NIC  CMI Herbarium Specimen 173935
Oidium caricaePowdery mildew of babacoCarica pentagoniaH1985IHNZHampshireCentral Science Laboratory records
Oidium cyclaminisPowdery mildew of cyclamenCyclamen sp.O1991NIC  Plant Health and Inspection Service – internal database
Oidium hyssopiPowdery mildew of hyssopHyssopus officinalisH1970NIC  Braun (1995) p. 224
Oidium neolycopersici*Powdery mildew of tomatoLycopersicon esculentumH1987IHNLSouth East EnglandFletcher et al. (1988); Kiss et al. (2001)
Oidium sp.Powdery mildew of akebiaAkebia quinataO2001NIC  Royal Horticultural Society, Wisley
Oidium sp.Powdery mildew of spiraeaSpiraea × bumaldaO1979NIC BuckinghamshireCentral Science Laboratory records
Oidium stapeliaePowdery mildew of stapeliaStapelia hanburyanaO1991NIC  Ing (1990a)
Pestalotia berberidisLeaf spot of berberisBerberis sp.O1989IHFRLondonCentral Science Laboratory records
Pestalotia palmorum Leaf spot of palmChamaerops sp.O1988IHNLLondonCentral Science Laboratory records
Pestolotia photiniaeLeaf spot and dieback of photiniaPhotinia sp.O 1984IHFRHampshireCentral Science Laboratory records
Pestalotiopsis versicolorLeaf spot of fuchsiaFuchsia sp.O1976NIC  ADAS; M.E. Upstone, personal communication
Phaeochora steinheilii Tar spot of leaves and petioles of dwarf palmChamaerops sp.O1999NIC  British Mycological Society Fungal Records Database
Phaeoramularia antipus Leaf spot of honeysuckleLonicera periclymenum ‘Serotina’O1988IHNLWest YorkshireCentral Science Laboratory records
Phloeosporella ceanothiLeaf spot and dieback of ceanothusCeanothus sp.O2001NIC  MAFF Quarterly Report Jan–Mar 2001
Phoma agnita Leaf spot of impatiensImpatiens (New Guinea)O2000IHNLLincolnshireCentral Science Laboratory records
Phoma loticolaDieback of bird's foot trefoilLotus corniculatusN1988IHNLLincolnshire.Plant Health and Inspection Service – internal database
Phoma telephiiLeaf spot, dieback and canker of sedumSedum telephium x spectabileO1986NIC CheshireCentral Science Laboratory records
Phoma valerianellae1Damping-off of common cornsaladValerianella olitoriaH1984ISFRWest SussexNathaniels (1985)
Phomopsis garryaeLeaf spot of garryaGarrya sp.O1986NIC  ADAS Wolverhampton, confirmed by CMI
Phomopsis theaeDieback of camelliaCamellia sp.O1983IHNZDevonCentral Science Laboratory records
Phyllachora shiraianaTar spot of bambooArundinaria linearisO2002NIC SurreySpooner (2004)
Phyllactinia maliPowdery mildew of mespilusAmelanchier grandifloraO1991NIC  Ing (1990a,b)
Physalacria cryptomeriaeNeedle spot of Japanese cedarCryptomeria japonicaO1975NIC GloucestershireLaessøe & Spooner (1993)
Podosphaera balsaminaePowdery mildew of orange balsamImpatiens noli-tangereO1995NIC  Tapster & Bailey (1975)
Podosphaera euphorbiae-hirtaePowdery mildew of bird cactusPedilanthus tithymaloidesO1991NIC  Ing (1990a)
Podosphaera ferrugineaPowdery mildew of salad burnetSanguisorba minor ssp. minorN1975NIC  Tapster & Bailey (1975)
Podosphaera helianthemiPowdery mildew of rock-roseHelianthemum pilosum var. purpureumO1975NIC  Tapster & Bailey (1975)
Podosphaera spiraeaePowdery mildew of meadowsweetFilipendula ulmariaN1990NIC  Ing (1990c)
Podosphaera thalictriPowdery mildew of meadow rueThalictrum aquilegifoliumO1991NIC  Ing (1991)
Podosphaera verbenae*Powdery mildew of verbenaVerbena lasiostachysO1994NIC KentCentral Science Laboratory – internal document
Podosphaera volkartiiPowdery mildew of mountain avensDryas octopetalaN1977NIC ScotlandDennis (1986); British Mycological Society Fungal Records Database
Pseudocercosporella anguioides*Eyespot of wheatTriticum aestivumA1986NIC HertfordshireBateman (1988)
Puccinia carthami1Rust of safflowerCarthamus tinctoriusA1975IS ScotlandCentral Science Laboratory records
Puccinia distincta*Rust of daisyBellis perennisO1973NIC West SussexPreece et al. (2000)
Puccinia heucheraeRust of heucheraHeuchera spp.O2004NIC SurreyHenricot et al. (2007)
Puccinia jussiaeaeRust of ludwigiaLudwegia arcuataO1978NIC  ADAS Cambridge, Disease Incidence Apr–Jun 1978
Puccinia longicornis Rust of bambooPseudosasa japonicaO1977NIC East SussexReid (1978)
Puccinia marianaRust of holy thistleSilybum marianumO1981NIC NorfolkGjaerum & Dennis (1997)
Ramichloridium piniDieback of pine shootPinus radiataT1982NIC ScotlandBritish Mycological Society Fungal Records Database
Ramichloridium verrucosumBlack lesions of stored cabbageBrassica oleracea var. capitataA1975NIC  Geeson (1975)
Ramularia bryoniaeLeaf spot of white bryonyBryonia dioicaN1997NIC SurreyPegler et al. (1999)
Ramularia collo-cygni*Leaf spot of spring barleyHordeum vulgareA1998NIC ScotlandAnonymous (1999)
Ramularia galegaeLeaf spot of goat's rueGalega officinalisO1999NIC SurreySpooner (2003)
Ramularia coriandri1Shoot necrosis of corianderCoriandrum sativumH1980ISINEssexCentral Science Laboratory records
Ramularia montanaLeaf spot of willow herbZauschneria californicaO2004NIC  Royal Horticultural Society, Wisley RHS
Sawadaea tulasneiPowdery mildew of mapleAcer palmatumO1990NIC  Ing (1990b)
Sclerotium hydrophilum*Leaf spot of giant waterlilyNymphaea giganteaO1994NIC LondonCentral Science Laboratory records
Septoria betulaeLeaf spot of downy birchBetula pubescensN2004NIC ScotlandGreen (2004)
Septoria cucurbitacearumLeaf spot of courgetteCucubita pepoH1982NIC JerseyBradshaw (1984)
Septoria elaeagniLeaf spot of elaeagnusElaeagnus ebbingiiO1985NIC HampshireCentral Science Laboratory records
Septoria polemoniiLeaf spot of Jacob's ladderPolemonium sp.N1995NIC  Central Science Laboratory records
Septoria soldanellaeLeaf spot of soldanellaSoldanella montanaO1978NIC HertfordshireCentral Science Laboratory records
Sirococcus pulcherNeedle lesions on spring heathErica carneaO1974NIC NorfolkCentral Science Laboratory records
Spermospora loliiLeaf spot of perennial ryegrassLolium perenneN1978NIC ShropshireMAFF Plant Pathologist's Quarterly Record 1978 No. 2, p. 6
Spilocaea photiniicolaScab of photinia leaves and berriesPhotinia × fraseriO1981IHNZSurreyCentral Science Laboratory records
Stemphylium sp.*Leaf spot of hebeHebe albicansO2003NIC YorkshireJones (2005)
Ulocladium atrumLeaf spot of cucumberCucumis sativus H1974NIC LancashireButler et al. (1979)
Urocystis bolivariLeaf smut of perennial rye-grassLolium perenneN1970NIC OxfordshireSpooner & Legon (2006)
Urocystis melicaeLeaf smut of wood melickMelica unifloraN1990NIC SurreySpooner & Legon (2006)
Ustilago echinataLeaf smut of reed Canary-grassPhalaris arundinaceaN1987NIC DevonSpooner & Legon (2006)
Ustilago scrobiculataLeaf smut of purple small-reedCalamogrostis canescensN1970NIC NorfolkSpooner & Legon (2006)
Oomycetes
Albugo amaranthiWhite rust of common amaranthAmaranthus retroflexusO1999NIC SurreySpooner (2001a)
Albugo tragopogonis var. inulaeWhite rust of ploughman's spikenardInula conyzaeN2001NIC SurreyLegon (2002)
Peronospora cytisi Downy mildew of laburnumLaburnum anagyroidesO1982NIC KentCentral Science Laboratory records (1953 report unconfirmed)
Peronospora erythraeaeDowny mildew of centauriumCentaurium erythraeaO1998NIC NorthamptonshirePreece (2002)
Peronospora hariotii*Downy mildew of buddlejaBuddleja globosaO1976IHFRSouth West EnglandCentral Science Laboratory records
Peronospora jaapiana Downy mildew of rhubarbRheum ×cultorumH1980NIC NorfolkCentral Science Laboratory records
Peronospora rubiDowny mildew of blackberryRubus fruticosusN1973NIC WalesCentral Science Laboratory records
Peronospora staticesDowny mildew of staticeLimonium sp.O1995IHNLCornwallHall et al. (1997)
Peronospora trigonellaeDowny mildew of fenugreekTrigonella foenum-graecumH1984IS BerkshireCentral Science Laboratory records
Phytophthora alni*Root and collar rot of alderAlnus glutinosaN1993NIC KentBrasier et al. (1995); Gibbs et al. (1999)
Phytophthora brassicaeStorage rot of cabbage leavesBrassica oleracea var. capitataA1978NIC  ADAS Advisory Plant Pathologists’ Conference
Phytophthora cinnamomi (A1 mating type)Dieback of camelliaCamellia sp.O1979NIC WalesCentral Science Laboratory records
Phytophthora citrophthoraDieback of dumb caneDieffenbachia sp.O1978NIC  Central Science Laboratory records
Phytophthora drechsleriRoot rot of sugarbeetBeta vulgaris subsp. vulgarisA1981NIC WalesBritish Mycological Society Fungal Records Database
Phytophthora fragariae var. rubi*Root rot of raspberryRubus idaeusH1987NIC ScotlandDuncan et al. (1987)
Phytophthora hibernalis Browning of Lawson's cypress (roots attacked)Chamaecyparis lawsonianaO1978NIC West MidlandsCentral Science Laboratory records
Phytophthora infestans (A2 mating type)*Late blight of potatoSolanum tuberosumA1983NIC ScotlandMalcolmson (1985)
Phytophthora idaea*Root rot of raspberryRubus idaeusH1987NIC ScotlandKennedy & Duncan (1995)
Phytophthora ilicis*Twig dieback of hollyIlex sp.N1989NIC East SussexStrouts & Winter (1994)
Phytophthora inflataRoot rot of elderSambucus tenuifoliumO1991NIC SuffolkHall et al. (1992)
Phytophthora kernoviae*Trunk canker of beechFagus sylvaticaN2003NIC CornwallBrasier et al. (2005)
Phytophthora ramorum*Dieback of viburnumViburnum tinusO2002IH West SussexLane et al. (2003)
Phytophthora sojae Root rot of Bath asparagusOrnithogalum pyrenaicumH1987NIC West SussexCentral Science Laboratory records
Plasmopara obducens*Downy mildew of impatiensImpatiens balsaminaO2003NIC East SussexLane et al. (2005)
Plasmopara ribicolaDowny mildew of blackcurrantRibes nigrumH1986NIC  Dennis (1986) p. 383
Pythium splendensBlack stem rot of pelargoniumPelargonium spp.O1970NIC West SussexGriffin (1972)
Pythium tracheiphilum*Stem infection of lettuceLactuca sativaH1988NIC YorkshireInternational Mycological Institute Herbarium Specimen 327877/8
Bacteria
Agrobacterium radiobacter (with Ri-plasmid)*Root mat of cucumberCucumis sativusH1974NIC EssexWeller et al. (2000)
Burkholderia gladioli pv. alliicola*Rot of onionAllium cepaA1974IHEWarwickshireTaylor (1975)
Clavibacter michiganensis subsp. sepedonicus*†Ring rot of potatoSolanum tuberosumA2003IHNLWalesDefra website
Dickeya dieffenbachiae*Leaf spot of dieffenbachiaDieffenbachia sp.O1971NIC  National Collection of Plant Pathogenic Bacteria
Dickeya zeae*Slow wilt of chrysanthemumChrysanthemum morifoliumO1970NIC East AngliaNational Collection of Plant Pathogenic Bacteria
Pseudomonas cichorii1Leaf spot of lettuceLactuca sativaH1971NIC  National Collection of Plant Pathogenic Bacteria
Pseudomonas corrugata1Pit necrosis of tomatoLycopersicon esculentumH1973NIC  National Collection of Plant Pathogenic Bacteria
Pseudomonas savastanoi pv. savastanoiRoot knot of neriumNerium oleanderO1988NIC  National Collection of Plant Pathogenic Bacteria
Pseudomonas syringae (probably pv. aesculi)*Bleeding canker of horse chestnutAesculus hippocastanumO2001NIC HampshireWebber (2005); J. Elphinstone, CSL, personal communication
Pseudomonas syringae pv. aptata1Bacterial leaf spot of sugar beetBeta vulgaris subsp. vulgarisA1987NIC  National Collection of Plant Pathogenic Bacteria
Pseudomonas syringae pv. berberidisLeaf spot of berberisBerberis spp.O1983NIC  National Collection of Plant Pathogenic Bacteria
Pseudomonas syringae pv. philadelphiLeaf spot of mock orangePhiladelphus coronariusO1982NIC  Roberts (1985)
Pseudomonas syringae pv. pisi1Bacterial blight of peaPisum sativumA1985ISNLLeicestershireCentral Science Laboratory records
Pseudomonas syringae pv. tagetis1Leaf spot of tagetesTagetes erectaO1970NIC  National Collection of Plant Pathogenic Bacteria
Pseudomonas syringae pv. tomato1Bacterial speck of tomatoLycopersicon esculentumH1973NIC WorcestershireNational Collection of Plant Pathogenic Bacteria
Pseudomonas syringae pv. viburniBacterial leaf spot of viburnumViburnum sp.O1986NIC  Stead et al. (2006)
Ralstonia solanacerum*1Brown rot of potatoSolanum tuberosumA1992NIC OxfordshireWalker (1992)
Rhizobium sp. (with Ri-plasmid)Root mat of cucumberCucumis sativusH1997NIC YorkshireWeller et al. (2005)
Xanthomonas arboricola pv. corylinaBacterial blight of hazelnutCorylus avellanaH1976NIC SomersetLocke & Barnes (1979)
Xanthomonas campestris ‘wallflower pathovar’Leaf spot and wilt of wallflowerErysimum cheiriO1970NIC South East EnglandGriffin & Baker (1976)
Xanthomonas campestris pv. incanae1Wilt of stocksMattiola incanaeO1990NIC  Sellar (1995); D. Stead, CSL, 2006, personal communication
Xanthomonas fragariae*†Angular leaf spot of strawberryFragaria×ananassaH2004IHNLKentP. Reed, CSL, 2006, personal communication
Xanthomonas translucens pv. graminisBacterial streak of Italian rye-grassLolium multiflorumP1978NIC  National Collection of Plant Pathogenic Bacteria
Phytoplasma       
‘Candidatus Phytoplasma prunorum’*†European stone fruit yellowsPrunus armenica, P. domesticaH2000IHEKentDavis & Adams (2000)
Viruses
Barley mild mosaic virus*Mosaic disease of barleyHordeum vulgarisA1986NIC WiltshireAdams et al. (1987)
Barley yellow mosaic virus*Yellow mosaic disease of barleyHordeum vulgarisA1980NIC OxfordshireHill & Evans (1980)
Bedford virus (Aubian wheat mosaic virus?)Stunting of wheatTriticum aestivumA1995NIC BedfordshireClover et al. (1999a), Hariri et al. (2001)
Beet necrotic yellow vein virus*Rhizomania disease of sugarbeetBeta vulgaris subsp. vulgarisA1987NIC SuffolkHill & Torrance (1989)
Beet pseudo-yellows virusInterveinal chlorosis disease of lettuceLactuca sativaH1987IHNLEast YorkshireCoffin & Coutts (1990)
Beet soil-borne virusBarney patch disease of sugarbeetBeta vulgaris subsp. vulgarisA1982NIC NorfolkHenry et al. (1986)
Beet yellow stunt virusStunting and death of lettuceLactuca sativaH1986NIC KentWright et al. (1989)
Blackberry chlorotic ringspot virusChlorotic mottle and ringspot of blackberryRubus fruticosusH1988NIC ScotlandJones et al. (2004; 2006); A.T. Jones, SCRI, UK, personal communication
Broad bean wilt virus 2Leaf mottle disease of ornamental foxgloveDigitalis sp.O2002NIC HampshireMumford et al. (2006); R. Mumford, CSL, UK, personal communication
Calibrachoa mottle virusLeaf mottle disease of million bellsCalibrachoa sp.O2003IHNLNorth YorkshireCentral Science Laboratory records
Canna yellow mottle virus*Leaf mottle disease of cannaCanna sp.O1999IH HampshireWright (1999)
Cocksfoot cryptic virusLatent infection of cocksfootDactylis glomerataP1994NIC ScotlandTorrance et al. (1994)
Cynosurus mottle virusMottle of crested dog's tailCynosurus cristatusP1970NIC YorkshireA’Brook (1972)
Hawaiian Rubus leaf curl virusLatent infection of blackberryRubus fruticosusH2003NIC ScotlandJones et al. (2004)
Holcus streak virusStreak of Holcus spp.Holcus mollisP and H. lanatusP1974NIC WalesCatherall & Chamberlain (1975)
Impatiens necrotic spot virus*Necrotic leaf lesions on cineriaCineraria sp.O1994IH East SussexWeekes et al. (1998)
Nemesia ring necrosis virusNecrotic ringspot disease of nemesiaNemesia spp.O2003NIC North West EnglandSkelton et al. (2004)
Oat chlorotic stunt virusChlorotic stunt disease of oatAvena sativaA1986NIC WalesBoonham et al. (1995)
Pepino mosaic virus*1Leaf mosaic disease of tomatoLycopersicon esculentumH1999ISNLEast YorkshireWright & Mumford (1999); Central Science Laboratory records
Petunia vein clearing virusVein clearing disease of petuniaPetunia hybridaO1996IH  Wright & Spence (1997)
Potato virus Y (NTN strain)*1Necrotic ring disease of potato tubersSolanum tuberosumA1990NIC  Wright (1992)
Raspberry bushy dwarf virus (RB strain)*1Bushy dwarf disease of raspberryRubus idaeusH1982NIC KentBarbara et al. (2001)
Rhododendron necrotic ringspot virusLeaf ringspot disease of rhododendronRhododendron sp.O1990NIC KentCentral Science Laboratory records
Soil-borne cereal mosaic virus*Stunting and necrotic fleck disease of wheatTriticum aestivumA1999NIC WiltshireClover et al. (1999b)
Tulip virus XChlorotic and necrotic leaf lesions of tulipTulipa sp.O1981NIC ScotlandMowat (1982)
Zucchini yellow mosaic virus*1Leaf mosaic disease of courgetteCucurbita pepoH1983ISUSJerseyWright et al. (1984)

The host documented is the host of first record. In some cases, this may not be the most important host. For example, Phytophthora ramorum was first recorded on a viburnum species (Viburnum tinus), but European beech (Fagus sylvatica) is a potentially much more significant host because it is a native tree. Hosts have been categorized as ornamental, horticultural crop, agricultural crop, wild native, exotic forestry tree or pasture plant for analysis. Sometimes, a host could be described under two categories, such as wild native and ornamental. The category chosen depended on the situation of the host when the pathogen was detected, such as whether in the field or in a nursery.

At least two scientists specializing in each pathogen group at CSL were asked to nominate those pathogens that were believed to be important in terms of economic and environmental damage or, if recently detected, potential to cause damage on host crops or ecosystems. A final decision was derived by consensus.

Numbers of pathogens introduced in 5-year periods from 1970 to 2004 were subject to linear regression analysis to determine if any trends were apparent.

Results

General

A list of new pathogens introduced into Great Britain from 1970 to 2004 together with a few newly identified endemic species that cannot be distinguished from introductions and any relevant information is presented in Table 1. The total number of new pathogens found was 234 including 157 fungi, 27 oomycetes (Peronospora, Phytophthora, Plasmopara and Pythium spp.), 26 viruses, 23 bacteria, and a single phytoplasma.

New records in 5-year periods from 1970 to 2004

An analysis of pathogens introduced during 5-year periods between 1970 and 2004 revealed a maximum of 48 in the period from 1975–1979 to a minimum of 22 in the period 1995–1999 (Fig. 1). No statistically significant trends related to new pathogens found in 5-year periods from 1970 to 2004 could be determined (S. Pietravalle, CSL, personal communication).

Figure 1.

Numbers of new plant pathogens introduced into Great Britain in 5-year periods from 1970 to 2004.

Types of new diseases and pathways of introduction

An analysis of the types of diseases caused by introduced fungi and oomyctes was undertaken from information presented in Table 1. Leaf and pine needle spots together with powdery mildews, white rusts (Albugo spp.), rusts and smuts, which primarily attack leaves, accounted for three-quarters of the diseases caused by newly recorded fungi and oomycetes (Fig. 2). It is likely that most of these pathogens were introduced with vegetative imports, such as seedlings, plants, budwood, rootstocks, bulbs, corms and tubers. For example, the A2 mating type of Phytophthora infestans was found in potato tubers imported from Egypt and on sale to the public in North Wales in May 1984 (Shaw et al., 1985). A2 isolates collected in 1981, 1982 and 1983 were later identified in culture collections indicating an even earlier introduction into Great Britain (Tantius et al., 1986). Whilst ware tubers are mostly consumed, it is a possibility that some tubers with latent infections could have been planted in allotments and gardens and produced blight-affected plants in the following season. Other fungal and oomycetes pathogens, such as Ascochyta imperfecta, the cause of leaf spot of lucerne (Medicago sativa), may have been introduced with seed.

Figure 2.

Diseases caused by new species of fungi and oomycetes introduced into Great Britain from 1970 to 2004.

Bacteria found for the first time between 1970 and 2004 caused rots of storage organs, such as bulbs and tubers, leaf spots and speckles, wilts and a trunk canker. The introduction of Pseudomonas syringae pv. pisi has been directly linked to an import of pea seed (Pisum sativum) (D. Stead, CSL, personal communication), but Clavibacter michiganensis subsp. sepedonicus was introduced with seed potato tubers, which are classified as vegetative imports. This pathogen, the cause of potato ring rot, is required to be eradicated under current quarantine legislation. The first outbreak of Ralstonia solanacearum in potato in Great Britain was linked to contaminated irrigation water from the river Thames. The water is believed to have become contaminated because of the release of bacteria from infected bittersweet (Solanum dulcamara) growing along the sides of the river. Discharge into the river system from a sewage works handling domestic waste, such as imported potatoes, may have been the original source of contamination for the bittersweet (J. Elphinstone, CSL, personal communication). Although R. solanacearum is eradicated when found in potato fields, it continues to survive in England along some watercourses (Elphinstone et al., 1998).

Viruses cause systemic diseases that produce mosaic, mottle, streak, necrotic spot, yellowing, vein clearing and stunting symptoms in infected plants. Virus names are descriptive and usually, but not always, indicate the main host and main type of symptom. Two, Pepino mosaic virus (PepMV) and Zucchini yellow mosaic virus (ZYMV) have been directly or indirectly linked to seed imports (Table 1). Others have gained entry with vegetative material.

Overall, 33 (~14%) of pathogens in Table 1 were found associated with imported vegetative material of host plants. Another 13 (~6%) were associated with seed imports. No information on the pathway of entry could be found for 188 (~80%) of pathogens.

Host plants affected by new pathogens

The types of host plant affected by new pathogens identified in Great Britain from 1970 to 2004 and documented in Table 1 are presented in Fig. 3. Just over half (123 of the 234), were first recorded on ornamentals. The second largest group, accounting for 37 new pathogen records, occurred on horticultural crops. There were 36 new records on wild native plants. This group includes native trees, such as elm and beech. Agricultural crops had 28 new records. Five new pathogens were identified on pasture plants and also on exotic tree species. No new records of bacteria and viruses were found on native plants or forestry tree species.

Figure 3.

Types of host plant first found affected by new plant pathogens introduced into Great Britain from 1970 to 2004.

Approximately 59% of all fungal records were from ornamentals and only ~17% were from agricultural and horticultural crops. This compares with ~44% of new oomycete records on ornamentals and ~37% identified on agricultural and horticultural crops. Approximately 42% of bacteria and phytoplasmas came from ornamentals and ~54% from food crops with ~31% of virus records coming from ornamentals and ~58% from food crops. Therefore, new records of bacteria and viruses were proportionally greater than fungi and oomycetes on agricultural and horticultural crops.

Although fluctuations in numbers of new records in each of these five-year periods were apparent, no obvious trends were evident on ornamentals and agricultural plus horticultural crops from 1970 to 2004 for each of the four major pathogen groups tabulated for each 5-year period (Tables 2 and 3). There has been no marked increase in pathogens being introduced on ornamentals or crop plants between 1970 and 2004. If anything, introductions on ornamentals have been steady since 1970 (Table 2) and there have been fewer introductions on crop plants since 1990 (Table 3).

Table 2.  Numbers of new pathogens in each pathogen group first found on ornamentals in each 5-year period from 1970 to 2004
5-year periodFungiOomycetesBacteria and phytoplasmasVirusesTotal
1970–1974 6 140 11
1975–197918 400 22
1980–198413 122 18
1985–198913 020 15
1990–199424 112 28
1995–1999 5 302 10
2000–200414 203 19
Total931299123
Table 3.  Numbers of new pathogens in each pathogen group first found on agricultural and horticultural plants in each 5-year period from 1970 to 2004
5-year periodFungiOomycetesBacteria and phytoplasmasVirusesTotal
1970–1974 4 0 5 0 9
1975–1979 7 1 1 0 9
1980–1984 7 4 0 415
1985–1989 3 5 2 515
1990–1994 2 0 1 2 5
1995–1999 4 0 1 3 8
2000–2004 0 0 3 1 4
Total2710131565

Six new pathogens were reported on tomato (Lycopersicon esculentum) and five each on lettuce and camellia (Camellia japonica). Sugarbeet (Beta vulgaris) and potato (Solanum tuberosum) had four new pathogens recorded whilst wheat (Triticum aestivum), barley (Hordeum vulgare), onion (Allium cepa), cucumber (Cucumis sativus), blackberry (Rubus fruticosus), pelargonium (Pelargonium spp.), and Corsican pine (Pinus nigra subsp. laricio) each had three.

Most ornamentals and about half the horticultural crops were growing under glass or polyethylene covers when pathogens were first found. Therefore, just over 50% of all new records occurred on plants in protected environments.

Countries of origin of introduced hosts of new pathogens

The countries of origin or the countries very strongly suspected as the origin of the host of new pathogens introduced into Great Britain from 1970 to 2004 are presented in Fig. 4. Only 36 records (~15%) have this information. A total of 17 pathogens either came from or were strongly suspected as coming from the Netherlands. New Zealand, France and the USA were also identified as sources. Four additional pathogens are very likely to have been introduced from Europe. The origin of the remainder of the pathogens cannot be established. Plasmopara obducens was likely to have been introduced with cuttings or seed of an Impatiens sp. (Jones & O’Neill, 2004), but these may have originated from Europe, Central or North America.

Figure 4.

Country of origin of the hosts on which new plant pathogens were introduced into Great Britain from 1970 to 2004. Percentages are derived from 36 records where country of origin was either known or strongly suspected.

First occurrence of new pathogens in Great Britain

Regions of Great Britain where new pathogens introduced from 1970 to 2004 were first recorded are given in Fig. 5. This analysis only takes into consideration those records where the location of the first finding is known. This amounts to 156 or two-thirds of the 234 pathogens listed in Table 1.

Figure 5.

Regions in Great Britain (Scotland, Wales and regions of England) where new plant pathogens introduced from 1970 to 2004 were first identified.

Fifty-nine pathogens were first recorded in the SE England. This region comprises the counties of Kent, East Sussex, West Sussex, Surrey, Hampshire, Berkshire, Oxfordshire and Buckinghamshire plus London and the Channel Islands. Twenty-two new pathogens were reported in the East Anglian region of eastern England, incorporating Norfolk, Suffolk, Essex, Hertfordshire, Bedfordshire and Cambridgeshire. In SW England (Gloucestershire, Wiltshire, Somerset, Devon and Cornwall), 17 new pathogens were recorded. Wales and other regions of England had fewer records including one from the Isle of Man included under NW England. Scotland recorded 23 new pathogens, mainly on crops important to this country, such as berry fruits and pine trees.

Important new pathogens

Many of the new pathogens reported for the first time in Great Britain between 1970 and 2004 caused very minor diseases to ornamentals or crop plants. However, some caused significant damage and were considered important (indicated by an asterisk in Table 1).

Table 4 shows that fewer important pathogens were found in the 1970s than in other decades. More were found in the 1980s and numbers since then have remained fairly constant. A smaller proportion (~10%) of the total recorded fungal pathogens was regarded as important compared with those in other groups (~37–41%). For this analysis, the only phytoplasma listed in Table 1 has been included with the bacterial pathogens.

Table 4.  Numbers of new pathogens identified as important in each pathogen group found in 5-year periods from 1970 to 2004
5-year periodFungiOomycetesBacteria and phytoplasmasVirusesTotal
1970–1974 1 04 0 5
1975–1979 1 10 0 2
1980–1984 4 10 3 8
1985–1989 2 40 2 8
1990–1994 4 11 2 8
1995–1999 3 00 3 6
2000–2004 1 34 0 8
Total161091045

In total, 45 (~19%) out of 234 new pathogens were considered important. Of these, the origins of five fungi, one oomycete, two bacteria and two viruses are recorded in Table 1. The Netherlands was the source or strongly suspected to be the source of five, the USA the source or suspected source of two and France the source of one. Two others originated from Europe, but the particular country could not be identified.

Fungi

Sixteen of the 157 fungal pathogens listed are regarded as important. Of these, 10 were found on ornamentals, four on agricultural crops and two on horticultural crops (Table 1). Three were powdery mildews (Erysiphe azaleae, Oidium neolycopersici and Podosphaera verbenae) and two were Fusarium spp.

Oomycetes

CSL specialists consider 10 of the 27 (~37%) pathogens in this group to be important, including seven Phytophthora species, two downy mildews (Peronospora sp. and Plasmopara sp.) and one Pythium sp. Three of the 10 occurred on ornamentals, three on horticultural crops, three on native trees and one on an agricultural crop. Of all the pathogen groups only newly introduced oomycetes have been identified as causing important diseases on native flora in Great Britain.

Bacteria and phytoplasmas

Nine of the 24 bacterial and phytoplasma pathogens, which amount to over a third of new records in this group, are regarded as important (Table 1) with three attacking ornamental crops, three recorded on agricultural crops and two identified from horticultural crops. The phytoplasma ‘Candidatus Phytoplasma prunorum’, affecting stone fruit was first reported in 2000, in Kent, SE England, but was likely to have been introduced many years before in budwood from mainland Europe.

Viruses

Ten (38%) out of 26 new viral records between 1970 and 2004 are regarded as important with five, three and two occurring on agricultural crops, horticultural crops and ornamentals respectively (Table 1). Four of the viruses were transmitted by soilborne plasmodiophoromycetes belonging to Polymyxa spp., two by aphids and one by a thrip. Another, PepMV, can be spread by bumblebee pollinators in glasshouses, as it is highly contagious. The other two viruses, Canna yellow mottle virus and RBDV-RB Strain, have no known vectors.

Discussion

This list of non-native pathogens introduced into Great Britain for the period 1970–2004 is unlikely to be complete. In investigating new pathogen entries, a wide variety of information sources was utilized, but since new records have been published in many places, it cannot be claimed that this search has been exhaustive. This study and its limitations suggest that a single body should take responsibility for collating and documenting all new pathogen records.

Between 1970 and 2004, there have been many advances in techniques for detection and diagnosis of plant pathogens, but at the same time there has been a decline in numbers of field- and laboratory-based plant pathologists in Great Britain. Over the same period, a closer liaison has developed between countries in the EU over quarantine issues and requirements with a corresponding conformity of regulations and changes in trade, as developing countries develop new agricultural and horticultural products for export. These factors will have influenced the likelihood of new plant pathogens being introduced and also their chances of being detected, but it is difficult to define their relative effects. Certainly, more emphasis has been placed recently on encouraging global trade and overcoming quarantine barriers by managing disease risks, which has led to greater access of plant products to EU markets.

The location of first record of a plant pathogen in Great Britain is not necessarily the first place of entry and establishment. It represents the first location that disease symptoms were recognized and specimens sent for diagnosis. In addition, some dates of first report may occur long after entry, for example, if their discovery occurred as a result of surveys for particular types of pathogen by a specialist. It is probable that some of the newly described pathogens found on ornamental and native species, such as some of the powdery mildews, are not related to new introductions, but rather to first discoveries of pathogens that may have been indigenous and previously overlooked. It has not been possible with some fungal pathogens, such as rusts, that produce long-lived, windblown aeciospores and urediniospores, to determine whether they were a result of an introduction of an infected plant or they arrived as airborne inoculum from the European continent or elsewhere.

The greater number of fungal pathogens recorded for the first time in Great Britain between 1970 and 2004 compared with pathogens in other groups may simply be because there are more known fungal species than oomycetes, bacteria, phytoplasmas and viruses. It may also be a reflection of the numbers of professional mycologists compared with those of bacteriologists and virologists working in plant pathology. However, the proportion of new fungal pathogens causing important diseases was low compared with pathogens in the other groups. Of those fungi that were regarded as important, over half affected ornamentals. Very little information is available on the present status of most minor diseases caused by fungi first identified in Great Britain between 1970 and 2004. More fungal pathogens were first recorded in the 1975 to 1979 period on all six categories of crops (Fig. 1) than in any other. This can be attributed in part to a new compilation of British records of dematiaceous hyphomycetes (Ellis, 1976) and to a consolidation of new records of many ornamental powdery mildews (Tapster & Bailey, 1975). Many of the individual reports in these publications could not be traced to the actual year of the original record. They most likely represent a collation of new records gathered over a number of years before publication.

The mean number of new pathogens found in Great Britain in 5-year periods since 1970 has been fairly constant with even a possibility of a trend towards reduced numbers of new introductions since 1994 (Fig. 1). With volumes of imported plant material, such as fresh fruit, vegetables, live plants and cut flowers, increasing significantly between 1970 and 2004 (Anonymous, 1993, 2005a,b) this might indicate either that imports are becoming healthier or that entry inspection procedures into Great Britain are becoming more effective or a combination of both. Another possible explanation is that, as more pathogens become established, the pool of exotic pathogens capable of establishing in Great Britain is diminishing. However, this trend may be being countered by the creation of new pathogens through interspecific hybridization, especially in the genus Phytophthora (Brasier et al., 1999; Webber & Brasier, 2005). As, in the main, only pathogens that have established into Great Britain have been considered in the analysis, it could also reflect recent successes in the eradication of some pathogens, such as Fusarium foetens and CSNV.

It seems likely that many newly recorded fungi and oomycetes gained entry with vegetative plant imports. Leaf-spotting pathogens were the most numerous (Fig. 2) and undoubtedly gained entry with introductions that had some leaf material. Others, such as downy mildews and stem/crown/root-attacking fungi could have entered on rooted cuttings. These types of plant introductions are the most dangerous, especially if transported in bulk. If possible, safer options would be by seed or tissue culture. Of the 26 virus pathogens listed in Table 1, only two have been linked to imported seed. Others may have been introduced with plants, cuttings or runners. A more remote possibility is that the insect vectors carrying viruses, such as Beet pseudo-yellows virus, Beet yellow stunt virus, Impatiens necrotic spot virus and ZYMV, were introduced into Great Britain with imported produce or plants. Some, like Barley mild mosaic virus and Barley yellow mosaic virus, are not seed-borne and are spread from plant to plant by soilborne vectors. It is unlikely that these pathogens would have been introduced with barley seedlings. They are more likely to have been introduced with their vectors in soil attached to farm machinery, soil-contaminated host seed or other agricultural/horticultural products, e.g. potatoes, root vegetables.

Most new pathogens were found on ornamentals (Fig. 3) and probably reflecting the greater amount of trade in this type of plant, which is introduced usually as vegetative material rather than seed. Bulk importations of ornamentals often occur as seedlings, cuttings or bulbs. Without any evidence of serious diseases on many ornamentals, importation into the EU from countries outside the EU and then subsequent movement within the EU to Great Britain has been relatively straightforward. Plants that are hosts of pathogens that cause serious diseases are subject to more stringent EU phytosanitary regulations. This may be reflected in the relatively lower numbers of pathogen introductions with crop and tree species (Fig. 3), which are often prohibited as EU imports, unless imported as seed or in tissue culture.

Approximately 47% of all new pathogens, whose introduction could be traced to a country, came from the Netherlands (Fig. 4). This is most likely because of its leading status in the EU for agricultural, horticultural and floriculture trade. Ornamentals destined for EU markets are either produced in the Netherlands or sold at Dutch markets after importation. As ornamentals make up a significant proportion of hosts of new British records, it is probably inevitable that the Netherlands is a source of new pathogens. As well as ornamentals, there is proof that some new diseases of crops, such as tomato, potato, pea, lettuce and strawberry, gained entry from the Netherlands. This also is not surprising given that the Netherlands is the leading European supplier of propagating material and seed, which are often imported from outside the EU. New Zealand, which has a similar climate to Great Britain, a similar ornamental flora and historical links to Great Britain, is another documented source. France, Great Britain's nearest neighbour on mainland Europe, and the USA, where many new cultivars of crop plants and ornamentals are developed, are also significant sources (Fig. 4).

The results indicate that most new pathogens may have first appeared in SE England (Fig. 5). This is probably because the climate and markets in this part of Great Britain makes it more suitable for protected ornamental and horticultural crops. More plants would have been imported into this region than elsewhere in the country. Also, important scientific gardens, such as Royal Botanic Gardens at Kew, Surrey, with plant disease specialists are located in this area.

The numbers of important pathogens found in Great Britain have also been fairly constant since the 1980s when there seemed a marked increase from the 1970s (Table 4). However, the specialists asked to nominate important pathogens may have had a tendency to classify recent introductions as more important than old ones. Also, with time, some pathogens believed to have the potential to cause damage when first introduced may not be such a serious problem when reviewed after a few years.

The most important conclusion from this analysis is that the number of new or important pathogens establishing in Great Britain does not appear to have been increasing in recent years. Although there may be a general impression that the rate of introductions of new non-native pests is increasing as a result of growing global trade and movement (Waage et al., 2005), this is not borne out by the results of this study. A second key conclusion is that over half of new findings were associated with ornamental plants. This suggests that ornamental plants, whose international movement is not as strictly controlled as that of crop plants, are a conduit for the dissemination of plant pathogens.

Although many new plant pathogens have been found on ornamentals, only a few are regarded as important. Most notable have been Phytophthora kernoviae and P. ramorum, which can also attack native trees. Until recently, Great Britain has been the only location where P. kernoviae has been found and it has been tempting to classify this species as an indigenous Phytophthora. Indeed, it was named after the old Cornish word for Cornwall. However, P. kernoviae has now been isolated in New Zealand from custard apple (Annona reticulata) growing in an orchard and also from soil in a kauri forest park (Anonymous, 2006a).

Many isolates of species in the Phytophthora genus may be moving in the ornamental shrub and amenity tree-trade, and new genetic combinations may be occurring at nurseries where material from diverse sources are grown in close proximity under conditions conducive for disease development. The appearance of new Phytophthora spp. in Great Britain in recent years adds weight to the argument that the spread of serious pathogens that threaten the environment may be a result of the world trade in ornamental nursery stock.

The introduction of some important pathogens can be traced to the importation of propagating/planting material, which should have been accompanied by a plant health certificate issued by plant health authorities in the exporting country addressing specific health requirements. The EU plant health directives rely heavily on country or area freedom of pathogens. Post-entry quarantine to detect latent infections or diseases that may be slow at developing symptoms is rarely undertaken. The health of imported plants, therefore, is largely dependent on the exporting country and the extent to which exports comply with EU requirements.

The existing system also cannot guarantee that every avenue of entry for pathogens is covered. Measures cannot be taken against unknown pathogens. Even in countries such as Australia, with a strict post-entry quarantine system, serious exotic pathogens still gain entry (e.g. Anonymous, 2006b; Croft & Braithwaite, 2006). It is also possible that many exotic pathogens may be being introduced on smuggled plant material and this pathway of introduction is very difficult to control. To try and prevent illegal entry, the clothes and luggage of travellers would need to be routinely searched and large fines imposed on those caught with any plant material subject to plant health controls. However, this is unlikely to happen on a large and effective scale because of practical, economic and political considerations.

In some circumstances, the risks posed by new pathogens may be realized too late. Pepino mosaic virus was first identified in Peru as a pathogen of pepino (Solanum muricatum) and, although tomato was known to be susceptible in tests, the risks were not fully appreciated. The virus appeared on tomato in the EU before it was even known that tomato could be a natural host. The threat that the virus posed to an important crop was not foreseen (Spence et al., 2006).

Another problem is that even when a significant threat is determined by risk analysis, it can take many years for the necessary legislation aimed at preventing the introduction or further spread of the causal pathogen to be passed. It was realized that there was a serious risk that CSNV could be introduced into the EU in chrysanthemum cuttings from Brazil (Jones et al., 2001). However, before legislation could be considered, the virus was found in England in 2002 on plants derived from such cuttings (Mumford et al., 2003). In addition, Tomato chlorosis virus (ToCV) and Tomato infectious chlorosis virus (TICV), which are whitefly-transmitted and have been identified by risk analysis as potentially serious, have spread to new EU countries while measures that might prevent or delay spread were under consideration. It must be remembered that action to prevent spread is also dependent on appropriate measures being feasible to implement. Controls on the movement of tomato seedlings between European countries needed to prevent dissemination of ToCV and TICV would be difficult to implement and enforce. A similar example is the case of Iris yellow spot virus (IYSV), which is thrips-transmitted and a serious problem in leek and onion. A risk analysis recommending that IYSV be declared an EU quarantine pathogen was produced in 2002 when its distribution within Europe appeared to be confined to Slovenia (Jones, 2002). However, IYSV has now been identified in France, Italy and Spain and its quarantine status has still not been resolved (J. Woodhall, CSL, personal communication).

Only about 20% of the new pathogens found in Great Britain between 1970 and 2004 have been recorded as being associated with known imports or were strongly suspected as being associated with known imports. This does not mean that completely unknown pathways were responsible for the introduction of the remainder of the new pathogens reported. A ‘most likely’ pathway can be derived from the biology of the pathogen and whether seed, seedlings, tubers, etc., are involved. However, the records indicate that pathogens can gain entry and establish without being noticed. Even if some pathogens were indigenous or arrived in Great Britain by the natural dispersal of spores from the continent, the results suggest that many pathogens are passing through the plant health system undetected on plant material.

In addition to smuggling, it seems that a certain number of exotic pathogens are evading the plant health screen in Great Britain because (i) there is a reliance on exporting countries to meet EU plant health requirements and their reliability to meet these requirements may not be 100%, (ii) the large volumes of ornamentals traded around the world cannot adequately be inspected/monitored and influxes of previously unknown pathogens (some of which can attack more important hosts) may occur on them from time to time and (iii) exotic pathogens may be introduced before risks become apparent and before legislation to prevent entry is passed. However, the number of new pathogens gaining entry has not increased in recent years. Nonetheless, as more plant material is sourced from new areas of production, such as Africa and the Far East, new risks may emerge and continued vigilance is required. Predicting invasions of non-indigenous plant pathogens is a developing science (Mack et al., 2002) and will become increasingly important in the future.

Acknowledgements

The main source of information on pathogen introductions has come from current and retired CSL specialists. Andrew Aspin, Paul Beales, Roger Cook, John Elphinstone, Charles Lane, Rick Mumford, David Stead, Simon Weller, James Woodhall and Daphne Wright are thanked for their help in compiling lists and in determining the importance of the impact of pathogens. Joan Webber of Forest Research is also thanked for her contribution. Advice on the manuscript offered by Julian Smith is appreciated. The support of the Plant Health Division of the Department for Environment, Food and Rural Affairs is acknowledged.

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