Cookies on Invasive Species Compendium

Like most websites we use cookies. This is to ensure that we give you the best experience possible.

Continuing to use www.cabi.org means you agree to our use of cookies. If you would like to, you can learn more about the cookies we use.

Datasheet

Cronartium flaccidum (Scots pine blister rust)

Summary

  • Last modified
  • 27 July 2017
  • Datasheet Type(s)
  • Documented Species
  • Pest
  • Natural Enemy
  • Preferred Scientific Name
  • Cronartium flaccidum
  • Preferred Common Name
  • Scots pine blister rust
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Fungi
  •     Phylum: Basidiomycota
  •       Subphylum: Pucciniomycotina
  •         Class: Pucciniomycetes
  • Summary of Invasiveness
  • C. flaccidum is a heteroecious rust fungus, completing different stages of its life cycle on different plants. Mating of haploid strains occurs on species of Pinus, followed by the production of aeciospore...

Don't need the entire report?

Generate a print friendly version containing only the sections you need.

Generate report

Pictures

Top of page
PictureTitleCaptionCopyright
Uredinia on underside of leaf of Paeonia sp.  Original X10.
TitleUredinia
CaptionUredinia on underside of leaf of Paeonia sp. Original X10.
CopyrightUSDA-ARS/Systematic Mycology & Microbiology Laboratory
Uredinia on underside of leaf of Paeonia sp.  Original X10.
UrediniaUredinia on underside of leaf of Paeonia sp. Original X10. USDA-ARS/Systematic Mycology & Microbiology Laboratory
Telia on underside of Paeonia officinalis leaf. Original X10.
TitleTelia
CaptionTelia on underside of Paeonia officinalis leaf. Original X10.
CopyrightUSDA-ARS/Systematic Mycology & Microbiology Laboratory
Telia on underside of Paeonia officinalis leaf. Original X10.
TeliaTelia on underside of Paeonia officinalis leaf. Original X10.USDA-ARS/Systematic Mycology & Microbiology Laboratory
Telia on underside of Vincetoxicum hirundinaria leaf. Original X25.
TitleTelia
CaptionTelia on underside of Vincetoxicum hirundinaria leaf. Original X25.
CopyrightUSDA-ARS/Systematic Mycology & Microbiology Laboratory
Telia on underside of Vincetoxicum hirundinaria leaf. Original X25.
TeliaTelia on underside of Vincetoxicum hirundinaria leaf. Original X25.USDA-ARS/Systematic Mycology & Microbiology Laboratory
Aecia of Endocronartium pini on twig of Pinus sylvestris. Original X7.5.
TitleAecia of Endocronartium pini
CaptionAecia of Endocronartium pini on twig of Pinus sylvestris. Original X7.5.
CopyrightUSDA-ARS/Systematic Mycology & Microbiology Laboratory
Aecia of Endocronartium pini on twig of Pinus sylvestris. Original X7.5.
Aecia of Endocronartium piniAecia of Endocronartium pini on twig of Pinus sylvestris. Original X7.5. USDA-ARS/Systematic Mycology & Microbiology Laboratory
Aecia on twig of Pinus sylvestris. Original X7.5.
TitleAecia on twig
CaptionAecia on twig of Pinus sylvestris. Original X7.5.
CopyrightUSDA-ARS/Systematic Mycology & Microbiology Laboratory
Aecia on twig of Pinus sylvestris. Original X7.5.
Aecia on twigAecia on twig of Pinus sylvestris. Original X7.5.USDA-ARS/Systematic Mycology & Microbiology Laboratory
Teliospores in telial column. Original X400. Note scale bar.
TitleTeliospores
CaptionTeliospores in telial column. Original X400. Note scale bar.
CopyrightUSDA-ARS/Systematic Mycology & Microbiology Laboratory
Teliospores in telial column. Original X400. Note scale bar.
TeliosporesTeliospores in telial column. Original X400. Note scale bar. USDA-ARS/Systematic Mycology & Microbiology Laboratory
Teliospores in telial column, with basidiospores. Original X200. Note scale bar.
TitleTeliospores
CaptionTeliospores in telial column, with basidiospores. Original X200. Note scale bar.
CopyrightUSDA-ARS/Systematic Mycology & Microbiology Laboratory
Teliospores in telial column, with basidiospores. Original X200. Note scale bar.
TeliosporesTeliospores in telial column, with basidiospores. Original X200. Note scale bar. USDA-ARS/Systematic Mycology & Microbiology Laboratory
Urediniospores. Original X1000. Note scale bar.
TitleUrediniospores
CaptionUrediniospores. Original X1000. Note scale bar.
CopyrightUSDA-ARS/Systematic Mycology & Microbiology Laboratory
Urediniospores. Original X1000. Note scale bar.
UrediniosporesUrediniospores. Original X1000. Note scale bar.USDA-ARS/Systematic Mycology & Microbiology Laboratory
Urediniospores. Original X400. Note scale bar.
TitleUrediniospores
CaptionUrediniospores. Original X400. Note scale bar.
CopyrightUSDA-ARS/Systematic Mycology & Microbiology Laboratory
Urediniospores. Original X400. Note scale bar.
UrediniosporesUrediniospores. Original X400. Note scale bar.USDA-ARS/Systematic Mycology & Microbiology Laboratory
Aeciospores. Original X400. Note scale bar.
TitleAeciospores
CaptionAeciospores. Original X400. Note scale bar.
CopyrightUSDA-ARS/Systematic Mycology & Microbiology Laboratory
Aeciospores. Original X400. Note scale bar.
AeciosporesAeciospores. Original X400. Note scale bar.USDA-ARS/Systematic Mycology & Microbiology Laboratory
Aeciospores. Original X1000. Note scale bar.
TitleAeciospores
CaptionAeciospores. Original X1000. Note scale bar.
CopyrightUSDA-ARS/Systematic Mycology & Microbiology Laboratory
Aeciospores. Original X1000. Note scale bar.
AeciosporesAeciospores. Original X1000. Note scale bar.USDA-ARS/Systematic Mycology & Microbiology Laboratory

Identity

Top of page

Preferred Scientific Name

  • Cronartium flaccidum (Alb. & Schwein.) G. Winter 1880

Preferred Common Name

  • Scots pine blister rust

Other Scientific Names

  • Cronartium asclepiadeum (Willd.) Fr. 1815
  • Cronartium nemesiae Vestergr. 1896
  • Cronartium paeoniae Castagne 1845
  • Cronartium pedicularis Lindr. 1900
  • Erineum asclepiadeum Willd. 1806
  • Peridermium cornui Rostr. ex Kleb. 1890
  • Sphaeria flaccida Alb. & Schwein. 1805

International Common Names

  • English: blister: pine rust; blister: Scotch pine rust; Cronartium rust; pine stem rust; resin canker; resin top disease: pine; resin: pine canker; resin-top; resin-top disease; scotch pine blister rust
  • Spanish: roya americana del grosellero; roya vesiculosa del pino
  • French: rouille americaine du groseillier; rouille de la pivoine; rouille vesiculeuse de l'ecorce du pin

Local Common Names

  • Finland: tervasroso
  • Germany: Keinzopt; Kiefernrindenblasenrost
  • Norway: tyritopp
  • Sweden: törskate

EPPO code

  • CRONFL (Cronartium flaccidum)
  • ENDCPI (Endocronartium pini)

Summary of Invasiveness

Top of page

C. flaccidum is a heteroecious rust fungus, completing different stages of its life cycle on different plants. Mating of haploid strains occurs on species of Pinus, followed by the production of aeciospores, which infect various species of herbaceous dicotyledons. An asexual stage producing urediniospores occurs on the dicotyledonous plants, followed by the production of teliospores, the sexual stage, that germinate to form basidiospores that infect pines thus completing the cycle. A closely-related autoecious rust, Endocronartium (Peridermium) pini, only infects Pinus hosts. C. flaccidum is known from Europe and parts of northern and eastern Asia; it is a Regulated Pest for the USA (USDA/APHIS, 2008). As an invasive in other temperate areas, this rust could be damaging on native and introduced pines or the alternate host species. The infections on pines develop slowly, therefore the fungus might be overlooked, such that accidental introduction of the rust could occur through the importation of conifer [Pinopsida] seedlings or trees.

Taxonomic Tree

Top of page
  • Domain: Eukaryota
  •     Kingdom: Fungi
  •         Phylum: Basidiomycota
  •             Subphylum: Pucciniomycotina
  •                 Class: Pucciniomycetes
  •                     Order: Pucciniales
  •                         Family: Cronartiaceae
  •                             Genus: Cronartium
  •                                 Species: Cronartium flaccidum

Notes on Taxonomy and Nomenclature

Top of page

The diverse interactions of this heteroecious fungus with its hosts have resulted in a complicated nomenclature. Several species of Cronartium were initially identified for the rust on the various dicotyledons that are primary hosts. An anamorph, Peridermium cornui, was described as the aecial form of one of these species (Cronartium asclepiadeum) that is now synonymized with C. flaccidum (Wilson and Henderson, 1966).

Another Peridermium species, Peridermium pini (Willd.:Pers.) Lev., was found to be autoecious, living only on pines [Pinus]. A separate Cronartium name was established for it, but this species came to be viewed, instead, as a race of C. flaccidum (Wilson and Henderson, 1966; Hiratsuka, 1968). Hiratsuka (1969) created the genus, Endocronartium, for such autoecious forms of Cronartium-related rusts. This genus forms units that are more closely related to distinct species of Cronartium than to each other (Vogler and Bruns, 1998). A number of studies have elucidated the close genetic relationship between the heteroecious C. flaccidum and the autoecious P. pini (Moricca et al., 1996; Moricca and Ragazzi, 1998; Vogler and Bruns, 1998; Kasanen et al., 2000; Hantula et al., 2002) as well as the difficulty of separating them on a morphological basis (Gibbs et al., 1988; Kasanen, 1997; Kaitera et al., 1999b).

Description

Top of page

C. flaccidum is a heteroecious rust, the spermogonial and aecial stages occurring on species of “hard” or two-needled pines, and the uredinial and telial stages on the leaves of herbaceous species in dicotyledonous families such as Asclepiadaceae, Paeoniaceae, and Scrophulariaceae.

Spermogonia: caulicolous, on cankers, under bark, flat, yellow, turning brown, exuding spermatia in orange droplets.

Aecia: caulicolous, blister-like, 2-7 mm diameter, single or confluent; peridium several cells thick, white, peridial cells rhomboid-ellipsoid, walls thick, verrucose. Aeciospores in chains, globose, ovoid to ellipsoid, or polygonal, verrucose except for a smooth area, 21-36 x 14-24 µm, orange-yellow; wall hyaline, thick, 2-4 µm; warts 1-2 µm high.

Uredinia: hypophyllous, scattered or in groups, blister-like, 100-300 µm diameter. Peridium hemispherical, opening by a central pore. Urediniospores single on pedicel, ellipsoid to ovoid, sparsely echinulate, 18-30 x 11-22 µm, yellow; wall hyaline, 1.5-2.5 µm thick.

Telia: hypophyllous, often developing in uredinia, erumpent; teliospores in chains, adhering in columns to 2 mm or more long, pale orange to cinnamon-brown. Teliospores ellipsoid to cylindrical, not separating, 20-64 x 6-16 µm, smooth, with yellowish wall 1-3 µm thick.

Basidiospores: globose-subglobose, smooth, 4-12 µm diameter, their production giving a whitish appearance to upper ends of telia.

See also Mordue and Gibson (1978), Ragazzi et al. (1987), and Kaitera et al. (1999b).

Endocronartium pini is an autoecious rust, generally considered a closely related form of C. flaccidum, cycling from pine to pine through the infection of needles by spores produced in aecia. These spores are morphologically aeciospores, but function as teliospores (Hiratsuka, 1969). Wilson and Henderson (1966) do not identify any morphological differences between the aecial stages of the two species. Hiratsuka (1968) reported that aeciospores of European isolates of E. pini germinated to produce, for the most part, determinate, septate, usually binucleate, but frequently uninucleate, germ tubes, whereas the aeciospores of C. flaccidum produced indeterminate, aseptate germ tubes that are more frequently binucleate. Subsequently, Gibbs et al. (1988), Kasanen (1997), and Kaitera et al. (1999b) suggested that these germ tube characteristics were not consistently different between the heteroecious and autoecious rusts, so that the aeciospores cannot be used to distinguished these species morphologically.

See also Kuprevich and Tranzschel (1957), Hiratsuka (1969), and Kasanen (1997).

Distribution

Top of page

C. flaccidum occurs in Europe and parts of northern and eastern Asia in the Northern Hemisphere (Smith et al., 1988; CABI, 1989). The autoecious form, Endocronartium pini, only occurs in Europe, according to Hiratsuka (1969), but Tai (1979) and Chen (2002) report it from China. Given the difficulty of distinguishing the two forms on Pinus without molecular examination or inoculation of dicotyledonous hosts (Hantula et al., 2002), some of the Asian reports might be erroneous. Azbukina (2008) expected to find E. pini in Siberia, but did not.

Distribution Table

Top of page

The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Continent/Country/RegionDistributionLast ReportedOriginFirst ReportedInvasiveReferenceNotes

Asia

ArmeniaPresentCMI, 1989; EPPO, 2014
AzerbaijanPresentCMI, 1989; EPPO, 2014
ChinaRestricted distributionChen, 2002; EPPO, 2014
-AnhuiPresentCheng et al., 1998
-GuizhouPresentJing and Wang, 1989; Chen, 2002
-HeilongjiangPresentCMI, 1989; Cheng et al., 1995; EPPO, 2014
-HenanPresentChen, 2002
-HubeiPresentJing and Wang, 1989; Chen, 2002
-JiangsuPresentCMI, 1989; EPPO, 2014
-JilinPresentCMI, 1989; EPPO, 2014
-LiaoningPresentCMI, 1989; EPPO, 2014
-Nei MengguPresentChen, 2002
-ShaanxiPresentJing and Wang, 1989; Jing et al., 1995; Cao et al., 2000; Zhuang and Wei, 2005
-ShanxiPresentCheng et al., 1998
-SichuanPresentCMI, 1989; Jing and Wang, 1989; EPPO, 2014
-TibetPresentChen, 2002
-YunnanPresentCMI, 1989; EPPO, 2014
-ZhejiangPresentCMI, 1989; EPPO, 2014
Georgia (Republic of)PresentCMI, 1989; EPPO, 2014
IndiaAbsent, invalid recordEPPO, 2014
JapanPresentCMI, 1989; EPPO, 2014
-HokkaidoPresent Not invasive Hiratsuka, 1932
-HonshuWidespreadKobayashi, 2007
-KyushuPresentKobayashi, 2007
KazakhstanPresentChurakov, 1989
Korea, DPRPresentEPPO, 2014
Korea, Republic ofPresentYi et al., 1985; CMI, 1989; Cho and Shin, 2004; EPPO, 2014
TaiwanPresentHiratsuka and Chen, 1991

Europe

AustriaPresentNativeWidder, 1941; CMI, 1989; EPPO, 2014
BelgiumPresentNativeCMI, 1989; EPPO, 2014
BulgariaWidespreadNative1960Widder, 1941; CMI, 1989; Denchev, 1995; EPPO, 2014
Czech RepublicWidespreadEPPO, 2014
Czechoslovakia (former)WidespreadNativeKlebahn, 1938; CMI, 1989; EPPO, 2014
DenmarkPresentNativeFerdinandsen and Jørgensen, 1938; Hylander et al., 1953; Buchwald NF et al., 1961; CMI, 1989; EPPO, 2014
EstoniaPresentNativeCMI, 1989; EPPO, 2014
FinlandWidespreadNative Invasive Liro, 1907; Liro, 1908; CMI, 1989; Hantula et al., 1998; Kaitera and Hantula, 1998; EPPO, 2014
Former USSRPresentRozhkov, 1975; Storozhenko, 1987; Leont'eva and Stenina, 1990
FrancePresentNativeCornu, 1886; CMI, 1989; EPPO, 2014
GermanyPresentNativeKlebahn, 1901; Klebahn, 1938; CMI, 1989; EPPO, 2014
GreecePresentNative Invasive Diamandis & de Kam, 1986; CMI, 1989; EPPO, 2014
HungaryWidespreadNativeCMI, 1989; Szabo, 1998; EPPO, 2014
IrelandAbsent, invalid recordEPPO, 2014
ItalyPresentNative Invasive Morionde, 1975; Raddi et al., 1979; Ragazzi and Moriondo, 1980; CMI, 1989; Moricca et al., 1996; EPPO, 2014
LatviaPresentNativeKuprevich and Transchel, 1957
LithuaniaPresentKuprevich and Transchel, 1957; EPPO, 2014
MontenegroPresentKaradzic and Vujanovic, 2009
NetherlandsPresentNativeHiratsuka, 1968; CMI, 1989; EPPO, 2014
NorwayWidespreadNative Invasive Jørstad, 1925; Hiratsuka, 1968; Roll-Hansen, 1973; CMI, 1989; EPPO, 2014
PolandPresentNativeCMI, 1989; Siwecki and Chojnacki, 1989; Mulenko et al., 2004; EPPO, 2014
PortugalPresent, few occurrencesEPPO, 2014
-AzoresPresentEPPO, 2014
-Portugal (mainland)PresentNativeGonçalves, 1936; CMI, 1989
RomaniaPresentNativeKlebahn, 1938; CMI, 1989; EPPO, 2014
Russian FederationRestricted distributionKuprevich and Transchel, 1957; EPPO, 2014
-Central RussiaPresentNativeKuprevich and Transchel, 1957
-Eastern SiberiaPresentNativeKuprevich and Transchel, 1957; EPPO, 2014
-Northern RussiaPresentNative Invasive CMI, 1989; Krutov, 1989
-Russia (Europe)Restricted distributionEPPO, 2014
-Russian Far EastPresentNativeCMI, 1989; Azbukina, 1995; Kakishima et al., 1995
-Southern RussiaPresentNativeKuprevich and Transchel, 1957
-Western SiberiaPresentNativeKuzmina and Kuz'Min, 2008; EPPO, 2014
SerbiaPresentEPPO, 2014
SloveniaPresentJurc, 2007
SpainPresentNativeCMI, 1989; EPPO, 2014
SwedenWidespreadNative Invasive Rennerfelt, 1943; Rennerfelt, 1947; Hiratsuka, 1968; Klingström, 1973; Martinsson and Nilsson, 1987; CMI, 1989; EPPO, 2014
SwitzerlandRestricted distributionNativeWidder, 1941; CMI, 1989; EPPO, 2014
UKRestricted distributionNativeWilson and Henderson, 1966; CMI, 1989; EPPO, 2014
-England and WalesRestricted distributionEPPO, 2014
-ScotlandPresentGreig, 1987; Greig and Sharpe, 1991; Pei and Gibbs, 1991
UkrainePresentNativeCMI, 1989; Dudka et al., 2004; EPPO, 2014
Yugoslavia (former)PresentNativeCMI, 1989
Yugoslavia (Serbia and Montenegro)PresentWidder, 1941

Risk of Introduction

Top of page

The risk of introduction of either form of this rust is greater for those temperate parts of the Southern Hemisphere, such as Australia, where introduced Pinus species are grown in plantations (Neumann and Marks, 1996). Single-aged monoculture populations could suffer epidemics, in particular, if trees are at a susceptible age and the autoecious Endocronartium pini form is introduced. In addition, dicotyledonous hosts for the heteroecious C. flaccidum are native to the temperate countries of the Southern Hemisphere (USDA-ARS, 2009). Other alternate hosts (Gentiana spp., Paeonia spp.) may be introduced as ornamentals and be grown near introduced ornamental pines.

North America has a significant number of stem rusts of the genera Cronartium, Endocronartium and Peridermium on its native species of three-needled pines (Sinclair and Lyon, 2005), which are in a different section of the genus Pinus from the European two-needled hosts (USDA-ARS, 2009). The ecological situation into which C.flaccidum might invade is therefore complex. Some evidence exists of resistance in the native pines (Raddi and Fagnini, 1978; Kaitera and Nuorteva, 2008). Nevertheless, native or introduced primary (telial) hosts for C.flaccidum are present in North America (USDA-ARS, 2009). Among the USDA/APHIS Regulated Plant Pests, Rossman et al. (2006) place this species in the category of “Threat to major crop plants and forest trees”. Accidental introduction of the rust as a latent infection in pines or on pine wood, appears more likely than on ornamental dicotyledons, but the continent has no lack of pines for planting and regulatory agencies have established phytosanitary procedures (USDA/APHIS, 2008; Canadian Food Inspection Agency, 2009).

Introduction of E. pini to new temperate regions would require importation of infected seedlings without quarantine or the occurrence of viable aecia on bark-bearing pine wood materials or products. Apparently, due to regulatory vigilance or other circumstances, this has not happened yet.

Habitat

Top of page

Moricca and Ragazzi (1996) found that C. flaccidum isolates had different cultural morphologies in different regions of Italy. Likewise, Gibbs et al. (1988) determined that Peridermium pini isolates from different parts of Great Britain have different culture morphologies. Kaitera et al. (1999a; 2005) identify C. flaccidum as occurring in southern Finland, whereas Endocronartium pini is found throughout the country. Nevertheless, the two forms can occur in the same or adjacent stands of P. sylvestris (Kaitera et al., 1999a).

Habitat List

Top of page
CategoryHabitatPresenceStatus
Terrestrial-managed
Managed forests, plantations and orchards Present, no further details Harmful (pest or invasive)
Terrestrial-natural/semi-natural
Natural forests Present, no further details Harmful (pest or invasive)

Hosts/Species Affected

Top of page

The commercially valuable aecial hosts of C. flaccidum, specifically two-needled pines of Europe and Asia, vary in susceptibility (Raddi and Fagnini, 1978;Kaitera and Nuorteva 2008). Scots pine, Pinus sylvestris, is the common host in northern Europe, but appears to be less susceptible than the Mediterranean species when tested in southern Europe (Raddi and Fagnini, 1978). The North American three-needled pines tested were found to be relatively resistant. Less is known about the pine species reported as hosts in China (Tai, 1979; Teng, 1996; Cao et al., 2000; Chen, 2002; Zhuang and Wei, 2005), Japan (Kobayashi et al., 2007), Korea (Cho and Shin, 2004) and Taiwan (Hiratsuka and Chen, 1991). Raddi and Fagnini (1978) did not observe spotting on needles of young plants of the Asian species, Pinus densiflora, Pinusmassoniana and Pinus tabuliformis, which were exposed to natural basidiospore inoculation in Italy; these species appeared to be resistant.

The telial hosts of C. flaccidum are herbaceous dicotyledonous plants in at least 10 families, as demonstrated by inoculation tests (Wilson and Henderson, 1966; USDA/APHIS, 2008; Kaitera et al., 2012). Some of the species are not native to the geographic range of the rust, and infection was observed in gardens (Goncalves da Cunha, 1936; Gjaerum, 1974; BPI, 2009). Specialized forms referred to as formae speciales varying with respect to pathogenicity to various dicotyledonous hosts have been identified in Europe (Smith et al., 1988), but inoculation tests (Kaitera and Hantula, 1998; Kaitera, 1999; Kaitera et al., 1999a) have indicated that C. flaccidum has low host specificity. Although differences in host susceptibility within a plant genus were noted (Kaitera, 1999; Kaitera et al., 1999a), the broad host range of C. flaccidum suggests that additional host species are likely to be susceptible. Thus, the rust was recently reported from Paeonia daurica in Ukraine (Dudka et al., 2004) and Siphonostegia chinensis in China (Zhuang and Wei, 2005).

Growth Stages

Top of page Vegetative growing stage

Symptoms

Top of page

Infection of pine needles may or may not cause yellow-red spots on needles (Ragazzi et al., 1986; Smith et al., 1988); spots may appear only after some months (Ragazzi, 1989). Spermogonia appear within 1 or 2 years (Ragazzi, 1989) or later on older trees (Smith et al., 1988). The fungus grows into the shoots, which become swollen, and aecia are produced after one or two additional years (Grieg, 1987). Cankers on stems also bear blister-like pustules, containing orange-yellow spores, especially at bases of branch whorls (Butin, 1995), and the perennial growth of the fungus results in concentric zones of sporulation. Stems are flattened and deformed (Butin, 1995). Resin is produced from the cankers and in the wood underlying it. If cankers on the trunk grow large enough or separate cankers meet, girdling of the stem may result in death of the top or of the entire tree (Smith et al., 1988). The “resin top” name of the disease derives from the combined death of the tree top with copious visible resin generation. However, years may be required for infections to have this effect (Grieg, 1987). On Pinus sylvestris in Finland, Kaitera (2000) found that the average size of lesions bearing aecia on three- to twenty-year-old stems was about 4 cm in length.

On primary hosts, scattered, small chlorotic or necrotic spots appear on the upper side of leaves, with orange uredinia and, later, bristle-like yellowish to red-brown telia below (Wilson and Henderson, 1966; Ragazzi et al, 1987; Kaitera, 1999; Kaitera and Nuorteva, 2006). Spots are sometimes limited by veins (Ragazzi et al., 1987).

List of Symptoms/Signs

Top of page

Leaves

  • abnormal colours
  • fungal growth
  • yellowed or dead

Stems

  • canker on woody stem
  • dieback
  • gummosis or resinosis
  • mould growth on lesion

Biology and Ecology

Top of page

Life Cycle

Teliospores in bristle-like telia on dicotyledonous primary host leaves germinate in spring to early summer and produce basidiospores that infect the young pine needles through stomates (Mordue and Gibson, 1978; Ragazzi et al., 1987). Mycelium grows through the needles into the cambium of stems and into the rays (Butin, 1995). Haploid spermogonia are the mating organs produced on shoots within 1 or 2 years; after fertilization, aecia are produced on the canker tissues during the summer of the next year or the year after that (Smith et al., 1988). Aeciospores are wind-blown to young leaves of herbaceous dicotyledons, where infection requires a film of free moisture; uredinia and telia develop on the lower sides of leaves (Ragazzi, 1983). Urediniospores are a repeating spore form, spreading the organism in multiple cycles to susceptible new leaves of the dicotyledonous hosts during the growing season. Telia develop in uredinia or directly from leaves (Ragazzi et al., 1987).

In the autoecious Endocronartium pini, the spores produced by aecia are capable of infecting pine directly, without an intervening telial stage. When free water is present, aeciospores germinate on needles and infect through stomates (Van der Kamp, 1970). Wounding of the stem can enhance infection (Wilson and Henderson, 1966; Gibbs et al., 1988), and infections through stem wounds are more damaging (Van der Kamp, 1970).

Genetics

Moricca et al. (1996) identified three regions of DNA with high similarity in C. flaccidum and E. pini isolates from Europe. The 5.8s ribosomal gene sequence was highly conserved, but some heterogeneity appeared in the ITS1 and ITS2 regions. Nevertheless, the same sequence variants occurred in isolates of both fungi. Moricca and Ragazzi (1998) observed virtually identical restriction fragment length polymorphism (RFLP) profiles, again, suggesting a high degree of affinity between the two fungi. A diagnostic difference between them, observed in single-strand conformation polymorphism (SSCP) analysis of a highly variable region, was of a type found in genetic analyses of differences within a species.

Hantula et al. (1998) also observed a high degree of similarity in two genetic regions in European C. flaccidum and E. pini. Results of additional tests using the two markers led Hantula et al. (2002) to consider the two forms to be the same species. For one highly variable marker, differentiation was lower between the two rusts than within populations of each form.

Reproductive Biology

The two rusts are separated on the basis of their reproduction, because E. pini is autoecious, lacking the stage of sexual recombination on any primary host (Wilson and Henderson, 1966; Hantula et al., 2002). On the other hand, Gibbs et al. (1988) reported infection of a dicotyledonous host invitro, with production of telia, by isolates considered to be the autoecious form. This suggests that E. pini may be “facultatively heteroecious”, although Hantula et al. (2002) consider this unlikely. Kasanen et al. (2000) found support for E. pini as homothallic, if not clonal, whereas allele distribution among aecia of C. flaccidum provided evidence of both heterothallic and homothallic matings.

The spermogonia of E. pini appear to be self-fertilizing or non-functional (Hantula et al., 2002). Spermogonial fluid was observed on only a few infected plants in tests in Finland (Kaitera and Nuorteva, 2008).

Physiology and Phenology

Three specialized types of C. flaccidum in Europe have been proposed depending on the telial host genera and varying in geographic distribution (Smith et al., 1988). Scientific attention has focused on f. sp. typica in western Europe. Kaitera (1999) identified new primary hosts in the genus Melampyrum (Scrophulariaceae, now Orobanchaceae) infected by C. flaccidum in Finland; their susceptibility to the other two formae speciales was not examined.

The pine blister rust organisms also exhibit variations in morphology in culture. Pei and Gibbs (1991) found two morphological types of colonies derived from aeciospores that corresponded to two regions of E. pini in Great Britain. Likewise, Moricca and Ragazzi (1996) observed two groupings of C. flaccidum isolates with different cultural characters that were correlated to their geographic origins in Italy.

Mittempergher and Raddi (1977) observed differences in regional sources of C. flaccidum in Italy. A montane isolate was more virulent on Pinus nigra from the same region than were isolates from other habitats. E.pini spore collections from different areas of Finland also differ in virulence on the pine host, but no significant differences were observed among three C. flaccidum collections (Kaitera and Nuorteva, 2008).

Associations

Insect may play a role in mating in C. flaccidum based on the similarity of its life cycle to that of Cronartium ribicola (Mordue and Gibson, 1978; Smith et al., 1988). In that species, insects are attracted to sweet liquid produced from spermogonia and appear to promote fertilization by carrying spermatia between them (Hunt, 1997).

Pappinen and von Weissenberg (1994) investigated an interaction between Pissodes piniphilus, the pine top weevil, and E. pini. The weevils fed more often on infected branches than on healthy branches, and the fungus may infect through feeding wounds, but results were inconclusive concerning the role for the insect as vector of the fungus.

E. pini is parasitized by the conidial fungus Tuberculina maxima (Wilson and Henderson, 1966; Gibbs et al., 1987), but that does not substantially affect losses due to rust (Moricca et al., 2001). Growth on the aecia apparently reduces sporulation rather than lesion expansion (Van der Kamp, 1970).

Climate

Top of page
ClimateStatusDescriptionRemark
Cs - Warm temperate climate with dry summer Preferred Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers
Cw - Warm temperate climate with dry winter Preferred Warm temperate climate with dry winter (Warm average temp. > 10°C, Cold average temp. > 0°C, dry winters)
Ds - Continental climate with dry summer Preferred Continental climate with dry summer (Warm average temp. > 10°C, coldest month < 0°C, dry summers)
Dw - Continental climate with dry winter Preferred Continental climate with dry winter (Warm average temp. > 10°C, coldest month < 0°C, dry winters)

Natural enemies

Top of page
Natural enemyTypeLife stagesSpecificityReferencesBiological control inBiological control on
Cladosporium tenuissimum Antagonist Spores
Tuberculina maxima Hyperparasite Fruit bodies/Spores

Notes on Natural Enemies

Top of page

Tuberculina maxima (van der Kamp, 1970) and Cladosporium tenuissimum (Moricca et al., 1999; 2001) are naturally occurring hyperparasites of C. flaccidum.

T. maxima invades C. flaccidum aecia, which reduces the formation and sporulation of aeciospores (van der Kamp, 1970; Gibbs et al., 1987). The fungus also infects the spermogonia of Cronartium spp. and has been found on Cronartium spp. uredinia and telia (Wicker, 1981). In the UK, T. maxima reduced the aecia production of E. pini by 30% (van der Kamp, 1970).

C. tenuissimum inhibits C. flaccidum aeciospore germination in vitro, parasitizes aeciospores and destroys their cell wall, probably using enzymes (Moricca et al., 2001).

No control measures are available in practice to use T. maxima or C. tenuissimum for reducing Cronartium spp. incidence on Pinus spp. (Wicker, 1981; Moricca et al., 2001).

Means of Movement and Dispersal

Top of page

Natural Dispersal

Rust aeciospores, urediniospores and sporidia (basidiospores) are distributed by wind (Alexopoulos et al., 1996; Hunt, 1997). Aeciospores and urediniospores may be disseminated greater distances than the basidiospores, which may be limited to less than 500 metres (Hunt, 1997).

Vector Transmission

An association of Endocronartium pini with pine top weevils may involve transmission, but results were inconclusive (Pappinen and von Weissenberg, 1994).

Accidental Introduction

Introduction of either form of the rust would be possible if seedlings or young trees were transported while the systemic infections were latent (USDA/APHIS, 2008).

Pathway Vectors

Top of page
VectorNotesLong DistanceLocalReferences
Plants or parts of plants Yes USDA/APHIS, 2008
Windaeciospores, urediniospores Yes Yes Smith et al., 1988

Plant Trade

Top of page
Plant parts liable to carry the pest in trade/transportPest stagesBorne internallyBorne externallyVisibility of pest or symptoms
Bark hyphae; spores Yes Yes Pest or symptoms not visible to the naked eye but usually visible under light microscope
Leaves hyphae; spores Yes Yes Pest or symptoms not visible to the naked eye but usually visible under light microscope
Stems (above ground)/Shoots/Trunks/Branches hyphae; spores Yes Yes Pest or symptoms not visible to the naked eye but usually visible under light microscope
Wood hyphae Yes Pest or symptoms not visible to the naked eye but usually visible under light microscope
Plant parts not known to carry the pest in trade/transport
Bulbs/Tubers/Corms/Rhizomes
Flowers/Inflorescences/Cones/Calyx
Fruits (inc. pods)
Growing medium accompanying plants
Roots
Seedlings/Micropropagated plants
True seeds (inc. grain)

Wood Packaging

Top of page
Wood Packaging not known to carry the pest in trade/transport
Loose wood packing material
Non-wood
Processed or treated wood
Solid wood packing material with bark
Solid wood packing material without bark

Impact Summary

Top of page
CategoryImpact
Economic/livelihood Negative

Impact

Top of page Severe epidemics on Pinus sylvestris caused by C. flaccidum have been reported in Sweden (Rennerfelt, 1943; 1947; Martinsson and Nilsson, 1987), Norway (Jørstad, 1925; Roll-Hansen, 1973), Finland (Kaitera et al., 1994; Kaitera, 2000; Kankaanhuhta et al., 2000), Germany (Klebahn, 1938), Greece (Diamandis and de Kam, 1986), UK (Wilson and Henderson, 1966; Murray et al., 1969; Gibbs et al., 1987; Greig, 1987), Russia (Krutov, 1989; Azbukina, 1995) and China (Jing and Wang, 1989). In Italy, C. flaccidum epidemics on Pinus nigra, Pinus pinea and Pinus pinaster were frequently reported from 1953 to 1972 (Moriondo, 1975).

In Finland, severe C. flaccidum epidemics have been reported in young P. sylvestris stands, with about 70% of trees infected (Kaitera, 2000). In some locations in Germany, 21-28% of P. sylvestris over 40 years of age were infected by C. flaccidum (Mülder, 1953). In northern Norway, Endocronartium pini affected 60% of P. sylvestris in some stands (Jørstad, 1925). In Thetford forest in England, UK, the number of P. sylvestris trees infected by E. pini increased from 1 to 10% from 1964 to 1979 (Greig, 1987). A C. flaccidum epidemic in Greece killed 5000 m³ of Pinus spp. trees over a 1000 ha area (Diamandis and de Kam, 1986).

In Sweden, E. pini and C. flaccidum caused 40-70% losses in radial increment in mature P. sylvestris stands (Martinsson and Nilsson, 1987). In northern Finland, E. pini reduced the volume of saw timber trees in mature P. sylvestris stands by 2% in trees bearing stem lesions and by 10% in trees with dead tops (Kaitera et al., 1994). The corresponding reductions in marketing value of saw timber trees were 18 and 15%, respectively (Kaitera et al., 1994). In Scotland, UK, E. pini occurred most frequently in old trees; over 50% of the stands infected by E. pini were more than 30 years old (Murray et al., 1969) and the annual loss in timber wood was 4500 m³. In Italy, C. flaccidum reduced the annual height increment more in severely affected P. nigra trees than in slightly affected trees in years of severe rust incidence (Mittempergher and Raddi, 1975).

Risk and Impact Factors

Top of page

Impact mechanisms

  • Pathogenic

Impact outcomes

  • Host damage
  • Negatively impacts forestry
  • Negatively impacts livelihoods
  • Reduced amenity values

Invasiveness

  • Abundant in its native range
  • Has a broad native range
  • Has high reproductive potential
  • Highly adaptable to different environments
  • Highly mobile locally
  • Long lived
  • Reproduces asexually

Likelihood of entry/control

  • Difficult to identify/detect as a commodity contaminant
  • Difficult to identify/detect in the field
  • Difficult/costly to control

Diagnosis

Top of page

Polymerase chain reaction (PCR)-amplified fragments of two regions of rDNA can be used in restriction fragment length polymorphism (RFLP) and single-strand conformation polymorphism (SSCP) analysis to distinguish alternating from non-alternating isolates of pine blister rust (Moricca and Ragazzi, 1998). Sequences for several regions of rDNA, particularly those for the 5.8s rRNA examined by Moricca et al. (1996), are currently available in GenBank for comparison (NCBI, 2009).

Detection and Inspection

Top of page

The delay of sporulation for months or years after infection of pines (Wilson and Henderson, 1966) reduces the reliability of single inspections of seedlings and young trees to detect this fungus. Spots may or may not result from infection of needles (Raddi et al., 1979; Ragazzi et al., 1986). Infection through wounded stems is also possible (Wilson and Henderson, 1966). Established infections produce cankers with blister-like aecia on stems or bark-bearing wood. In the field, nearby herbaceous alternate hosts can be examined for the presence of uredinia and/or bristle-like telial columns on the undersides of leaves (Kaitera et al., 2005).

Similarities to Other Species/Conditions

Top of page

Hantula et al. (2002) showed that C. flaccidum and the autoecious rust Endocronartium pini are genetically almost indistinguishable despite differences in life cyle. The two cannot be distinguished by aeciospore morphology (Kasanen, 1997; Kaitera et al., 1999b). Inoculation tests on the dicotyledonous alternate hosts should establish the difference (Kaitera, 1999; Kaitera et al., 1999a; Kaitera and Nuorteva, 2008, but see Gibbs et al., 1988). Moricca and Ragazzi (1998) identified a restriction fragment length polymorphism (RFLP) technique that distinguished the two forms on the basis of one electrophoretic band resulting from Hinf1 restriction endonuclease digestion of the IGS1 region of rDNA.

In North America, there are at least 11 species of Cronartium including Cronartium ribicola and six species of Peridermium that infect trees in the genus Pinus (Sinclair and Lyon, 2005). To a certain extent, these can be distinguished by aeciospore and urediniospore morphology, as well as by symptomatology. Some cause stem cankers, and other rusts produce galls or witchs’ brooms in infected stems or branches. Others cause no stem symptoms at all (Sinclair and Lyon, 2005). Although some of the common Eurasian hosts have been naturalized e.g. Pinus sylvestris (USDA-NCRS, 2009), tests indicate that the three-needled pines native to North America are not susceptible to C. flaccidum (Raddi and Fagnini, 1978; Kaitera and Nuorteva, 2008). Cronartium comandrae, a widespread North American pine stem rust that also infects introduced two-needled species, also hosts for C. flaccidum, produces unique tear-drop-shaped aeciospores on pine (Sinclair and Lyon, 2005).

Other European rusts that can attack pines have a heteroecious life cycle similar to that of C. flaccidum, but usually infect different alternate hosts. Coleosporium tussilaginis, the pine needle rust, shares a few telial hosts with the blister rust, but produces its spermogonia and aecia on pine needles, not on stems (Smith et al., 1988). Also, teliospores of this rust on species of Melampyrum are single and cylindrical, produced not in long columns, but in waxy crusts (Wilson and Henderson, 1966). Melampsora populnea infects the shoots of two-needled pines, causing shoot bending and/or tip death (Smith et al., 1988). Its linear aecia lack a peridium and the aeciospores are significantly smaller than those of C. flaccidum (Wilson and Henderson, 1966).

Although their aeciospores cannot be distinguished even at the level of scanning electron microscopy (Kasanen, 1997), the invasive species C. ribicola does not infect the primary hosts of C. flaccidum in Europe (Kaitera and Nuorteva, 2006) or the same species of pines, because it is restricted to five-needled (soft) pines (Sinclair and Lyon, 2005). Butin (1995) notes that C. flaccidum tends to infect at the top of a tree rather than at the base of stems or of lower branches, where C. ribicola infection is usually found.

Prevention and Control

Top of page

Prevention

Given the possibility of latent infections in Pinus, phytosanitary post-entry quarantine of any imported plants is necessary (USDA/APHIS, 2008). Accidental introduction would also likely be prevented by controlling bark-bearing wood in shipping materials from areas where the rust occurs (see Canadian Food Inspection Agency, 2009: MAF, 2009).

Eradication

Butin (1995) recommends removal of infected branches or trees in stands where the disease is already present. Pruning of infected branches may or may not prevent development of additional cankers on the trunk, although the general purpose of removing inoculum is achieved (Moricca and Ragazzi, 2008).

Control

Cultural control and sanitary measures

Basidiospores are disseminated only over a short distance (Hunt, 1997), therefore removal of the primary hosts from the vicinity of limited plantings of pine is a measure that can reduce infection by the heteroecious C. flaccidum (Mordue and Gibson, 1978; Butin, 1995). In Italy, the alternate host is too common for this effort to be effective or worthwhile; however, development of a “hazard map” of the known distribution of the alternate host allows for planting of susceptible pines away from sources of inoculum (Moricca and Ragazzi, 2008).

Chemical control

The use of fungicides may be practical for rust control on plantation, nursery and garden trees, but is impractical in forests (Moricca and Raghazzi, 2008).

Biological control

The hyperparasite Cladosporium tenuissimum is proposed by Moricca et al. (2001) as a possible means of control for stem rust. The aeciospores are directly penetrated and parasitized by the conidial fungus. Tests on two-year-old pine seedlings in the greenhouse showed that treatment with the parasite prevented new rust infections by an average of 42%.

Host resistance

Selection of more resistant species or provenances of pines for growing in areas of stem blister rust is a feasible and promising means of control; although Moricca et al. (2001) state that breeding efforts were not successful. The testing methodology may be a major factor in the usefulness of results obtained. Because the fungus develops slowly even in susceptible plants, progress in rating the plants for resistance must be slow.

Raddi and Fagnini (1978) used three methods to inoculate seedlings and young plants of different pine species with basidiospores of C. flaccidum. Species from southern Europe were susceptible whereas North American and Asian species appeared resistant. In later tests, differing levels of susceptibility were found in three of the European species (Raddi et al., 1979) and results indicated that selection for resistance might be possible in Pinus pinaster.

Although P. sylvestris appeared resistant in the limited tests in Italy (Raddi and Fagnani, 1978),it is a major host species in northern Europe, and differences in susceptibility have been observed (Mordue and Gibson, 1978). Over a number of years, Kaitera and Nuorteva (2008) tested seedlings 1-7 years old with aeciospores of E. pini and basidiospores of C. flaccidum. Little disease was obtained and no significant differences among provenances of Finnish trees were observed. The apparent resistance of the introduced American species Pinus contorta in the same tests led the researchers to recommend use of that species as an alternative to Pinus sylvestris in Finland.

Although levels of rust disease caused by both forms were low (10% or less), Kuzmina and Kuz’min (2008) did find variation in the resistance of “climatypes” of P. sylvestris from different parts of Russia in trials in Western Siberia. Soil type and humidity affected the severity of disease as well as the strength of the provenance tests.

Among the several alternate hosts of C. flaccidum, differences in susceptibility would be expected as well. Roll-Hansen (1973) found strong resistance in some Paeonia (ornamental peony) cultivars and suggested that use of those in gardens could assist in control of C. flaccidum. Kaitera et al. (1999a) also observed variation in susceptibility among telial hosts in several genera, including Paeonia, but found the rust to have a low host specificity in general, because infections by Finnish isolates occurred on both native and non-native species.

Gaps in Knowledge/Research Needs

Top of page

Additional information is needed on variation within C. flaccidum as well as on its relationship with Endocronartium pini. The existence of specialized forms with respect to pathogenicity on telial hosts and/or on the pine species should be investigated beyond western Europe, particularly in Asia, where available host species differ.

References

Top of page

Alexopoulos CJ; Mims CW; Blackwell M, 1996. Introductory Mycology. Fourth edition. New York, New York, USA: John Wiley and Sons, Inc, 868 pp.

Azbukina ZM, 1995. Cronartium species on Pinus species in the Russian far east. In: Kaneko S, Katsuya K, Kakishima M, Ono Y, eds. Proceedings of the 4th IUFRO Rusts of pines Working Party Conference, Tsukuba, Japan, 65-69.

Azbukina ZM, 2008. Taxonomical notes on species of Cronartium (Uredinales) occurring in Russia. Mikologiya i Fitopatologiya, 42(1):3-12.

Bagyanarayana G, 1989. Rusts of pine from India. In: Hiratsuka Y, Samoil JK, Blenis PV, Crane PE, Laishley BL, eds. Rusts of Pine. Proceedings of the IUFRO Rusts of Pine Working Party Conference, Canada. Forestry Canada, 333-337.

BPI (US National Fungus Collections), 2009. Fungal Databases - Specimens. Beltsville, USA: Systematic Mycology and Microbiology Laboratory, Agricultural Research Service, USDA. www.nt.ars-grin.gov/fungaldatabases/specimens/specimens.cfm

Buchwald NF et al., 1961. Lists of parasitical fungi and of hosts of such fungi: Denmark, Finland, Norway, Sweden. I. Pinus, Populus, Quercus. Medd. Norsk. Skogfors°ksvesen, 17.

Butin HH, 1995. Tree diseases and disorders: causes, biology, and control in forest and amenity trees. Oxford, UK; Oxford University Press, x + 252 pp.

Cao ZhiMin; Li ZhenQi; Zhuang JianYun, 2000. Uredinales from the Qinling Mountains. Mycosystema, 19(1):13-23.

CFIA, 2008. Wood packaging. Wood packaging. Ottawa, Canada: Government of Canada, unpaginated. http://www.inspection.gc.ca/english/plaveg/for/cwpc/wdpkge.shtml

Chen MM, 2002. Forest fungi phytogeography: Forest fungi phytogeography of China, North America, and Siberia and international quarantine of tree pathogens. Sacramento, USA: Pacific Mushroom Research and Education Center, 469 pp.

Cheng DongSheng; Xue Yu; Pan XueRen; Li WuHan, 1998. Population genetic structures of three Cronartium species from China based upon allozyme analysis. Mycosystema, 17(1):32-39; 15 ref.

Cheng DS; Xue Y; Shao LP, 1995. Differentiation among Cronartium species from northeast China by isozyme analysis. In: Proceedings of the Fourth Rusts of Pines Working Party Conference, Tsukuba. Tsukuba, Japan: Institute of Agriculture and Forestry, University of Tsukuba, 71-75.

Cho WD; Shin HD, 2004. List of plant diseases in Korea. Fourth edition. Seoul, Republic of Korea: Korean Society of Plant Pathology, 779 pp.

Churakov BP, 1989. Infection of different forms of Scots pine by phytopathogenic fungi. Lesovedenie, No. 1:69-73

CMI, 1989. Cronartium flaccidum. Distribution Maps of Plant Diseases, No. 616, edition 1. Wallingford, UK: CAB International.

Cornu M, 1886. Nouvel exemple de gTnTrations alternantes chez les champignons urTdinTes (Cronartium asclepiadeum et Peridermium pini corticolum). Paris, France: C.R. Hebd. Acad. Sc., 102:930-932.

Denchev CM, 1995. Bulgarian Uredinales. Mycotaxon, 55:405-465

Diamandis S; Kam Mde, 1986. A severe attack of Scots pine by resin top disease in N. Greece. European Journal of Forest Pathology, 16(4):247-249

Dudka IO; Heluta VP; Tykhonenko YY; Anrianova TV; Hayova VP; Prydiuk MP; Dzhagan VV; Isikov VP, 2004. Fungi of the Crimean Peninsula. Kiev, Ukraine: National Academy of Sciences of Ukraine, 452 pp.

EPPO, 2014. PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://www.eppo.int/DATABASES/pqr/pqr.htm

Epstein L; Buurlage MB, 1988. Nuclear division in germinating pciospores and its taxonomic significance for the western gall rust fungus, Peridermium harknessii. Mycologia, 80(2):235-240

Ferdinandsen C; Jørgensen CA, 1938. Skovtraeernes sygdomme. København, Denmark: Nordisk Forlag.

Gibbs J, 1997. Resin top disease. In: Compendium of conifer diseases [ed. by Hansen, E. M.\Lewis, K. J.]. St. Paul, Minnesota, USA: American Phytopathological Society, 30-31.

Gibbs JN; England N; Wolstenholme R, 1988. Variation in the pine stem rust fungus Peridermium pini in the United Kingdom. Plant Pathology, 37(1):45-53

Gibbs JN; Greig BJW; Hickman IT, 1987. An analysis of Peridermium stem rust of Scots pine in Thetford Forest in 1984 and 1985. Forestry, 60:204-218.

Gjaerum HB, 1974. Nordens Rustsopper (Northern rust species.). Oslo, Norway: Fungiflora., 321 pp.

Gonçalves Da Cunha A, 1936. Uredineae of Portugal. (Uredineas de Portugal.) Bol. Soc. broteriana, 11:169-265 pp.

Gregory SC, 1977. The effect of Peridermium pini (Pers.) Lev. on water conduction in Pinus sylvestris L. European Journal of Forest Pathology, 7(6):328-338

Greig BJW, 1987. History of Peridermium stem rust of Scots pine (Pinus sylvestris L.) in Thetford Forest, East Anglia. Forestry, 60:193-202.

Greig BJW; Sharpe AL, 1991. Pine stem rust (Peridermium pini) in a Scots pine provenance trial at Teindland forest. Scottish Forestry, 45(3):169-174

Grzywacz A; Wazny J, 1973. The impact of industrial air pollutants on the occurrence of several important pathogenic fungi of forest trees in Poland. European Journal of Forest Pathology, 3(3):129-141

Gäumann E, 1959. Die Rostpilze Mitteleuropas. Bern, Switzerland: Buchler & Co.

Haack G, 1914. Der Kienzopf (Peridermium pini (Willd.) Kleb.). Seine _bertragung von Kiefer zu Kiefer ohne Zwischenwirt. Zeitschrift fnr Forst- und Jagdwesen, 46:3-46.

Hantula J; Kasanen R; Kaitera J; Moricca S, 2002. Analyses of genetic variation suggest that pine rusts Cronartium flaccidum and Peridermium pini belong to the same species. Mycological Research, 106(2):203-209; 28 ref.

Hantula J; Niemi EM; Kaitera J; Jalkanen R; Kurkela T, 1998. Genetic variation of the resin top fungus in Finland as determined by random amplified microsatellites (RAMS). European Journal of Forest Pathology, 28(6):361-372; 13 ref.

Hertz M, 1930. Tutkimus mSnnyn tervasroson kehityksestS ja vaikutuksista. Communicationes Instituti Forestalis Fenniae, 15:1-40.

Hiratsuka N, 1932. Inoculation experiments with some heteroecious species of the Melampsoraceae in Japan. Japanese Journal of Botany, 6:1-33.

Hiratsuka N; Chen ZC, 1991. A list of Uredinales collected from Taiwan. Transactions of the Mycological Society of Japan, 32:3-22.

Hiratsuka Y, 1968. Morphology and cytology of aeciospores and aeciospore germ tubes of host-alternating and pine-to-pine races of Cronartium flaccidum in northern Europe. Canadian Journal of Botany, 46:1119-1122.

Hiratsuka Y, 1969. Endocronartium, a new genus for autoecious pine stem rusts. Canadian Journal of Botany, 47:1493-1495.

Hiratsuka Y, 1995. Pine stem rusts of the world-frame work for a monograph. In: Kaneko S, Katsuya K, Kakishima M, Ono Y, eds. Proceedings of the 4th IUFRO Rusts of pines Working Party Conference, Tsukuba, Japan, 1-8.

Hunt R, 1997. Stem rusts. In: Compendium of conifer diseases [ed. by Hansen, E. M.\Lewis, K. J.]. St. Paul, Minnesota, USA: American Phytopathological Society, 26.

Hylander N; Jrstad I; Nannfeldt JA, 1953. Enumeration uredionea rum scandinavicarum. Opera Botanica, 1:1-102.

Jing Y; Li WH; Zhao SG, 1995. Study on pine rusts in Northwest China. In: Kaneko S, Katsuya K, Kakishima M, Ono Y, eds. Proceedings of the Fourth IUFRO Rusts of Pines Working Party Conference, Tsukuba. Tsukuba, Ibaraki, Japan: Laboratory of Plant Pathology & Mycology, University of Tsukuba, 37-41.

Jing Y; Wang P, 1989. A study of the blister rust of Pinus massoniana of China. In: Hiratsuka Y, Samoil JK, Blenis PV, Crane PE, Laishley BL, eds. Rusts of Pine. Proceedings of the IUFRO Rusts of Pine Working Party Conference, Canada. Forestry Canada, 302-312.

Jurc D, 2007. Diseases of shoots, branches and trunk. Gremeniella abietina, Cronartium flaccidum, Melampsora pinitorqua. (Bolezni poganjkov, vej in debla. Gremeniella abietina, Cronartium flaccidum, Melampsora pinitorqua.) Gozdarski Vestnik, 65(2):89-104. http://www.dendro.bf.uni-lj.si/gozdv.html

Jørstad I, 1925. Norske skogsykdommer I. Nsletresykdommer bevirket av rustsopper, ascomyceter og fungi imperfecti. Meddelanden fra det Norske skogforsøksvesen, 62:19-186.

Kaitera J, 1999. Cronartium flaccidum fruitbody production on Melampyrum spp. and some important alternate hosts to pine. European Journal of Forest Pathology, 29(6):391-398; 23 ref.

Kaitera J, 1999. The effect of storage temperature, time and spore source on the germination of Cronartium flaccidum and Peridermium pini aeciospores in vitro. Karstenia, 39:69-75.

Kaitera J, 2000. Analysis of Cronartium flaccidum lesion development on pole-stage Scots pines. Silva Fennica, 34(1):21-27; 30 ref.

Kaitera J, 2002. Short-term effect of thinning on Pinus sylvestris damage and sporulation caused by Cronartium flaccidum. Scandinavian Journal of Forest Research, 17(2):158-165; 33 ref.

Kaitera J; Aalto T; Jalkanen R, 1994. Effect of resin-top disease caused by Peridermium pini on the volume and value of Pinus sylvestris saw timber and pulpwood. Scandinavian Journal of Forest Research, 9(4):376-381

Kaitera J; Fedorkov A; Jalkanen R; Krutov V; Tsvetkov V, 1995. Occurrence of Gremmeniella abietina damage on Scots pine along a pollution gradient from Monchegorsk nickel smelter to western Lapland. European Journal of Forest Pathology, 25(1):13-23

Kaitera J; Hantula J, 1998. Melampyrum sylvaticum, a new alternate host for pine stem rust Cronartium flaccidum. Mycologia, 90(6):1028-1030; 19 ref.

Kaitera J; Hiltunen R; Samils B, 2012. Alternate host ranges of Cronartium flaccidum and Cronartium ribicola in northern Europe. Botany, 90(8):694-703. http://www.nrcresearchpress.com/doi/full/10.1139/b2012-039

Kaitera J; Nuorteva H, 2003. Cronartium flaccidum produces uredinia and telia on Melampyrum nemorosum and on Finnish Vincetoxicum hirundinaria. Forest Pathology, 32:1-9.

Kaitera J; Nuorteva H, 2006. Finnish Cronartium ribicola does not infect alternate hosts of Cronartium flaccidum. Forest Pathology, 36(4):247-252.

Kaitera J; Nuorteva H, 2008. Inoculations of eight Pinus species with Cronartium and Peridermium stem rusts. Forest Ecology and Management, 255(3/4):973-981. http://www.sciencedirect.com/science/journal/03781127

Kaitera J; Nuorteva H; Hantula J, 2005. Distribution and frequency of Cronartium flaccidum on Melampyrum spp. in Finland. Canadian Journal of Forest Research, 35(2):229-234. http://pubs.nrc-crnc.gc.ca/.

Kaitera J; SeitamSki L; Hantula J; Jalkanen R; Kurkela T, 1999. Inoculation of known and potential alternate hosts with Peridermium pini and Cronartium flaccidum aeciospores. Mycological Research, 103(2):235-241; 27 ref.

Kaitera J; SeitamSki L; Hantula J; Jalkanen R; Kurkela T, 1999. Morphological variation of Peridermium pini and Cronartium flaccidum aeciospores. Mycological Research, 103(6):677-683; 33 ref.

Kakishima M; Imazu M; Katsuya K; Azbukina ZM; Ono Y; Kaneko S; Hiratsuka Y; Sato S, 1995. Preliminary survey of pine blister rusts in the Russian Far East. In: Kaneko S, Katsuya K, Kakishima M, Ono Y, eds. Proceedings of the Fourth IUFRO Rusts of Pines Working Party Conference, Tsukuba. Tsukuba, Ibaraki, Japan: Laboratory of Plant Pathology & Mycology, University of Tsukuba, 49-63.

Kankaanhuhta V; MSkisara K; Tomppo E; Piri T; Kaitera J, 2000. Monitoring of diseases caused by Heterobasidion annosum and Peridermium pini in Norway spruce and Scots pine stands by airborne imaging spectrometry (AISA). MetsSntutkimuslaitoksen tiedonantoja, 782:113-131.

Karadzic D; Vujanovic V, 2009. Aleppo pine defence against Sphaeropsis sapinea, Cronartium flaccidum and other fungal pathogens in the Mediterranean part of Montenegro. Glasnik ?umarskog Fakulteta, Univerzitet u Beogradu, No.99:59-74. http://user.sezampro.yu/~sf.bg

Kasanen R, 1997. Aeciospores of Cronartium flaccidum, C. ribicola and Endocronartium pini show no differences in morphology. European Journal of Forest Pathology, 27(4):251-260; 21 ref.

Kasanen R; Kaitera J; Hantula J, 2000. The genetic structure of Peridermium pini and Cronartium flaccidum cankers on Scots pine as revealed by two multi-allelic loci. Forest Pathology, 30:221-230.

Klebahn H, 1901. Kulturversuche mit Rostpilzen X. Zeitschrift fnr Pflanzenkrankheiten, 11:132-151.

Klebahn H, 1905. Kulturversuche mit Rostpilzen XII. Zeitschrift fnr Pflanzenkrankheiten, 15:65-108.

Klebahn H, 1907. Kulturversuche mit Rostpilzen XIII. Zeitschrift fnr Pflanzenkrankheiten, 17:129-157.

Klebahn H, 1914. Kulturversuche mit Rostpilzen XV. Zeitschrift fnr Pflanzenkrankheiten, 24:1-32.

Klebahn H, 1916. Kulturversuche mit Rostpilzen XVI. Zeitschrift fnr Pflanzenkrankheiten, 26:257-277.

Klebahn H, 1918. Peridermium pini (Willd.) Kleb. und seine _bertragung von Kiefer zu Kiefer. Flora, 11:194-207.

Klebahn H, 1924. Kulturversuche mit Rostpilzen XVII. Zeitschrift fnr Pflanzenkrankheiten, 34:289-303.

Klebahn H, 1938. Offene Fragen und neue Beobachtungen nber die rindenwohnenden Blasenroste der Kiefern nebst Bemerkungen nber einige andere Rostpilze. Zeitschrift fnr Pflanzenkrankheiten, 48:369-410.

Klingström A, 1973. Studies on free amino acid contents in the aeciospores of Endocronartium pini and Cronartium flaccidum. European Journal of Forest Pathology, 3:209-214.

Kobayashi T, 2007. Index of Fungi Inhabiting Woody Plants in Japan. Host, Distribution and Literature. Tokyo, Japan: Zenkoku-Noson-Kyiku Kyokai Publishing Co., 1227 pp.

Krutov VI, 1989. Gribnye bolezni hvoinyh porod v iskusstvennyh tsenozah taejnoi zony Evropeiskogo Severa SSSR: Petrozavodsk.

Kuprevich V; Transchel V, 1957. Cryptogamic plants of the USSR, Vol. IV, Rust Fungi. No. 1, Family Melampsoraceae. Moscow, USSR: USSR Academy of Sciences.

Kuzmina NA; Kuz'Min SR, 2008. Intraspecific response of Scots pine (Pinus sylvestris L.) to pathogens in a provenance trial in middle Siberia. Eurasian Journal of Forest Research, 11-2:51-59.

Lagerberg T, 1912. Studier ÷fver den norrlSndska tallens sjukdomar, sSrskildt med hSnsyn till dess f÷ryngring. Meddelanden frsn Statens Skogsf÷rs÷ksanstalt, 9:135-170.

Laundon GF, 1976. Peridermium (Fungi). Taxon, 25:186-187.

Leont'eva SI; Stenina NP, 1990. Phytopathological state of pine and spruce forests cultivated in the north-west of the Russian Federation. Mikologiya i Fitopatologiya, 23(4):389-392

Liese J, 1936. Zur Frage der Vererbbarkeit der rindenbewohnenden Blasenrostkrankheiten bei Kiefer. Zeitschrift fnr Forst- und Jagdwesen, 68:602-609.

Liro JI, 1907. Kulturversuche mit Finnischen Rostpilzen. II. Acta Societatis Pro Fauna et Flora Fennica, 29:1-58.

Liro JI, 1908. Uredinae Fennicae. Bidrag till kSnnedom af Finlands natur och folk, 65:1-567.

MAF, 2009. Search results - Endocronartium pini., New Zealand: Biosecurity New Zealand, Ministry of Agriculture and Forestry., unpaginated. http://www.biosecurity.govt.nz/search/node/Endocronartium+pini

Martinsson O; Nilsson B, 1987. The impact of Cronartium flaccidum on the growth of Pinus sylvestris. Scandinavian Journal of Forest Research, 2(3):349-357

Mittempergher L; Raddi P, 1975. Relationship between vigour and susceptibility of Austrian Pine (Pinus nigra) to blister rust (Cronartium flaccidum). European Journal of Forest Pathology, 5(1):44-49

Mittempergher L; Raddi P, 1977. Variation of diverse sources of Cronartium flaccidum. European Journal of Forest Pathology, 7(2):93-98

Mnlder D, 1953. Die Disposition der Kiefer fnr den Kienzopfbefall als Kernproblem waldbautechnischer Abwehr. Schriftenreihe der Forstlichen FakultSt der UniversitSt G÷ttingen und Mitteilungen der NiedersSchsischen Forstlichen Versuchsanstalt, 10:1-35.

Mordue JEM; Gibson IAS, 1978. Cronartium flaccidum. CMI Descriptions of Pathogenic Fungi and Bacteria, No. 580.Wallingford, UK: CAB International.

Moricca S; Kasuga T; Mitchelson K; Ragazzi A; Diamandis S, 1996. Heterogeneity in intergenic regions of the ribosomal repeat of the pine-blister rusts Cronartium flaccidum and Peridermium pini. Current Genetics, 29(4):388-394; 41 ref.

Moricca S; Ragazzi A, 1994. Axenic culture of the aecial state of Cronartium flaccidum from Italy. Mycological Research, 98(11):1258-1262

Moricca S; Ragazzi A, 1996. Culture characteristics and variation of Cronartium flaccidum isolates. Canadian Journal of Botany, 74(6):924-933.

Moricca S; Ragazzi A, 1998. Use of RFLP and SSCP analysis to differentiate the pine rusts Cronartium flaccidum and Peridermium pini. Mycological Research, 102(6):666-670; 27 ref.

Moricca S; Ragazzi A, 2008. Biological and integrated means to control rust diseases. In: Integrated Management of Plant Pests and Diseases, 3 [ed. by Ciancio, A.\Mukerji, K. G.]. Dordrecht, The Netherlands: Springer, 303-329.

Moricca S; Ragazzi A; Mitchelson KR, 1999. Molecular and conventional detection and identification of Cladosporium tenuissimum on two-needle pine rust aeciospores. Canadian Journal of Botany, 77(3):339-347; 32 ref.

Moricca S; Ragazzi A; Mitchelson KR; Assante G, 2001. Antagonism of the two-needle pine stem rust fungi Cronartium flaccidum and Peridermium pini by Cladosporium tenuissimum in vitro and in planta. Phytopathology, 91(5):457-468; 59 ref.

Morionde F, 1975. Characteristics of epidemics of blister rust of pines, Cronartium flaccidum (C. asclepiadeum), in Italy. Annali, Accademia Italiana di Scienze Forestali, 24:331-406

Mulenko W; Kozlowska M; Salata B, 2004. Microfungi of the Tatra National Park. A checklist., Poland: W. Szafer Institute of Botany, Polish Academy of Sciences, 72 pp.

Murray JS; Millar CS; van der Kamp BJ, 1969. Incidence and importance of Peridermium pini (Pers.) LTv. in North-east Scotland. Forestry, 42:165-184.

NCBI, 2009. Entrez cross-database search engine. Maryland, USA: National Center for Biotechnology Information. http://www.ncbi.nlm.nih.gov/sites/gquery

Neumann FG; Marks GC, 1990. Status and management of insect pests and diseases in Victorian softwood plantations. Australian Forestry, 53(2):131-144; 49 ref.

Olembo TW, 1971. A study on the mode of infection of Pinus sylvestris L. by Peridermium pini (Pers.) LTv. Forestry, 44:67-79.

Pappinen A; Weissenberg Kvon, 1994. The ability of the pine-top weevil to carry spores and infect Scots pine with Endocronartium pini. European Journal of Forest Pathology, 24(5):258-263

Pei MH; Gibbs JN, 1991. Cultural variation in Peridermium pini from two parts of the United Kingdom. European Journal of Forest Pathology, 21(3):164-167

Pei MH; Pawsey RG, 1991. Axenic culture of Peridermium pini. Mycological Research, 95(1):108-115

Raddi P; Fagnani A, 1978. Relative susceptibility to blister rust caused by Cronartium flaccidum of several species of pine. European Journal of Forest Pathology, 8(1):58-61

Raddi P; Fagnani A, 1981. Blister rust in maritime pine. European Journal of Forest Pathology, 11(3):187-190

Raddi P; Mittempergher L; Moriondo F, 1979. Testing of Pinus pinea and P. pinaster progenies for resistance to Cronartium flaccidum. Phytopathology, 69(6):679-681

Ragazzi A, 1983. Development of Cronartium flaccidum (Alb. et Schw.) Wint. on Vincetoxicum officinale Moench in connection with some environmental factors. Phytopathologische Zeitschrift, 108(2):160-171

Ragazzi A, 1986. Cronartium flaccidum (Alb. et Schw.) Wint.: susceptibility of Vincetoxicum officinale Moench. in relation to the age of leaves. Phytopathologia Mediterranea, 25(1-3):101-102

Ragazzi A, 1989. Past, present and future of Cronartium flaccidum in Italy. Phytopathologia Mediterranea, 28(1):5-9.

Ragazzi A, 1992. Production of telia by Cronartium flaccidum from infections with aecidiospores and with urediospores. Phytopathologia Mediterranea, 31(2):123-125

Ragazzi A; Dellavalle Fedi I; Mesturino L, 1989. The effects of some variables on the production of uredia and telia of Cronartium flaccidum. Phytopathologia Mediterranea, 28(1):43-45

Ragazzi A; Fagnani A; Dellavalle Fedi I, 1987. Telial and basidiospore stages of Cronartium flaccidum: light and scanning electron microscopy observations. Phytopathologia Mediterranea, 26(2):113-116

Ragazzi A; Fedi ID, 1992. Penetration of Cronartium flaccidum into pine needles. European Journal of Forest Pathology, 22(5):278-283

Ragazzi A; Fedi ID; Mesturino L, 1986. Cronartium flaccidum (Alb. et Schw.) Wint. spores: temperature requirements for germination. Phytopathologia Mediterranea, 25(1-3):57-60

Ragazzi A; Fedi ID; Mesturino L, 1986. Cronartium flaccidum on Pinus spp.: relation of inoculum concentration to symptom development. European Journal of Forest Pathology, 16(1):16-21

Ragazzi A; Mesturino L, 1986. The possibility of Vincetoxicum officinale infection by pciospores of Cronartium flaccidum (Alb. et Schw.) Wint. at high temperatures. Phytopathologia Mediterranea, 25(1-3):73-75

Ragazzi A; Moricca S; Dellavalle I, 1995. Growth of axenic cultures of Cronartium flaccidum on callus tissue from Pinus nigra var. laricio and Pinus sylvestris. European Journal of Forest Pathology, 25(1):31-37

Ragazzi A; Moricca S; Dellavalle I, 1998. Disease gradient of Cronartium flaccidum on its intermediate host Vincetoxicum hirundinaria. Zeitschrift fu^umlaut~r Pflanzenkrankheiten und Pflanzenschutz, 105(1):58-63; 16 ref.

Ragazzi A; Moriondo F, 1980. Results of Cronartium flaccidum (Alb. & Schw.) Wint. inoculations on eight-year-old plants of Pinus pinea L. In: Powers HR, Grasso V, Raddi P, ed. Phytopathologia Mediterranea, 19:51-56

Rennerfelt E, 1943. Om vsr nuvarande kunskap om t÷rskatesvampen (Peridermium pini) och sSttet f÷r dess spridning och tillvSxt. Svenska Skogsvsrdsf÷reningens Tidskrift, 41:305-324.

Rennerfelt E, 1947. Om f÷rekomsten av blssroststadiet i Peridermium-angripna tallbestsnd. Meddelanden frsn Statens Skogsforskningsinstitut, 6:191-215.

Roll-Hansen F, 1973. Resistance of Paeonia cultivars to Cronartium flaccidum in Norway. European Journal of Forest Pathology, 3:142-145.

Rossman AY; Britton K; Luster D; Palm M; Royer MH; Sherald J, 2006. Evaluating the threat posed by fungi on the APHIS List of Regulated Plant Pests. Plant Health Progress, May:1-3. http://www.plantmanagementnetwork.org/php/

Rozhkov AA, 1975. Resin canker. Zashchita Rastenii, No.1:44-45

Sinclair WA; Lyon H, 2005. Diseases of Trees and Shrubs. Second edition. Ithaca, USA: Cornell University Press, 660 pp.

Siwecki R; Chojnacki B, 1989. Epidemiology of Scots pine rusts in Poland. In: Hiratsuka Y, Samoil JK, Blenis PV, Crane PE, Laishley BL, eds. Rusts of pine. Proceedings of the IUFRO Rusts of Pine Working Party Conference, Canada. Forestry Canada, 158-163.

Smith IM; Dunez J; Lelliott RA; Phillips DH; Archer SA, 1988. European Handbook of Plant Diseases. Oxford, UK: Blackwell Scientific Publications, 583 pp.

Storozhenko VG, 1987. Fungus diseases in recreation forests. Lesnoe Khozyaistvo, No. 3:63-65

Szabo I, 1998. Occurrence and importance of rust fungi in Hungarian forests. Finnish Forest Research Institute, Research Paper, 712:9-13.

Tai FL, 1979. Sylloge Fungorum Sinicorum. Beijing, China: Science Press Academica Sinica, 1527 pp.

Teng SC, 1996. Fungi of China [ed. by Korf RP]. Ithaca, USA: Mycotaxon Ltd, xiv + 586 pp.

USDA/APHIS, 2008. Circular 34: Diseases of Picea spp. Post-entry Quarantine Manual for State Inspectors. Washington DC, USA: USDA, 10-152. http://www.aphis.usda.gov/import_export/plants/manuals/domestic/downloads/postentry.pdf

USDA-ARS, 2009. Germplasm Resources Information Network (GRIN). Online Database. Beltsville, Maryland, USA: National Germplasm Resources Laboratory. https://npgsweb.ars-grin.gov/gringlobal/taxon/taxonomysearch.aspx

USDA-NRCS, 2008. The PLANTS Database. Baton Rouge, USA: National Plant Data Center. http://plants.usda.gov/

van der Kamp BJ, 1968. Peridermium pini (Pers.) LTv. and the resin-top disease of Scots pine. I. A review of the literature. Forestry, 41:189-198.

van der Kamp BJ, 1970. Peridermium pini (Pers.) LTv. and the resin-top disease of Scots pine. III. Infection and lesion development. Forestry, 43:73-88.

Vogler DR; Bruns TD, 1998. Phylogenetic relationships among the pine stem rust fungi (Cronartium and Peridermium spp.). Mycologia, 90(2):244-257.

Wicker EF, 1981. Natural control of white pine blister rust by Tuberculina maxima. Phytopathology, 71(9):997-1000

Widder F, 1941. Untersuchungen nber forstschSdliche Cronartium-arten. +sterreichlicher Botanischer Zeitschrift, 90:107-117.

Wilson M; Henderson DM, 1966. British rust fungi. Cambridge, UK: Cambridge University Press.

Yi CK; Kim HJ; La YJ, 1985. Cronartium flaccidum found on Pinus densiflora in Korea. In: Ko JH, La YJ, eds. Proceedings of the Joint Conference IUFRO Working Party on Forest Gall Midges and Rusts of Pines. Suweon, Korea: Korean Forestry Society, 149-161.

Zhuang JY; Wei SX, 2005. Urediniomycetes, Uredinales. In: Fungi of Northwestern China [ed. by Zhuang, W. Y.]. New York, USA: Mycotaxon Ltd, 233-290.

Contributors

Top of page

19/08/09 Updated by:

Systematic Mycology & Microbiology Laboratory, USDA-ARS, 10300 Baltimore Ave., Beltsville, MD 20705, USA

Distribution Maps

Top of page
You can pan and zoom the map
Save map
Download KML file Download CSV file
Creative Commons Licence
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 3.0 Unported License.

Please click OK to ACCEPT or Cancel to REJECT

Creative Commons Licence
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 3.0 Unported License.

Please click OK to ACCEPT or Cancel to REJECT