Cronartium ribicola (white pine blister rust)
- Summary of Invasiveness
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- History of Introduction and Spread
- Risk of Introduction
- Hosts/Species Affected
- Host Plants and Other Plants Affected
- Growth Stages
- List of Symptoms/Signs
- Biology and Ecology
- Notes on Natural Enemies
- Means of Movement and Dispersal
- Pathway Vectors
- Plant Trade
- Environmental Impact
- Impact: Biodiversity
- Threatened Species
- Risk and Impact Factors
- Detection and Inspection
- Similarities to Other Species/Conditions
- Prevention and Control
- Links to Websites
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Cronartium ribicola J.C. Fisch.
Preferred Common Name
- white pine blister rust
Other Scientific Names
- Peridermium indicum Colley & M.W. Taylor
- Peridermium kurilense Dietel
- Peridermium strobi Kleb.
International Common Names
- English: currant rust
- Spanish: moho ampolla del piño blanco
- French: rouille vésiculeuse du pin blanc
- Chinese: wu zhen song pao xiu bing
Local Common Names
- Austria: Johannisbeeren-Säulenrost; Strobenrost; Weymouthskieferen-Blasenrost
- Germany: Johannisbeeren-Säulenrost; Strobenrost; Weymouthskieferen-Blasenrost
- Liechtenstein: Johannisbeeren-Säulenrost; Strobenrost; Weymouthskieferen-Blasenrost
- Macedonia: rgja po korata na petoiglichestite borovi
- Switzerland: Johannisbeeren-Säulenrost; Strobenrost; Weymouthskieferen-Blasenrost
- CRONRI (Cronartium ribicola)
Summary of InvasivenessTop of page C. ribicola infects white pines and Ribes spp., causing severe long-term damage and disruption to ecosystems by altering patterns of natural succession.
There are a total of 14 species of Pinus and over 40 susceptible Ribes species. Among the most susceptible pines in the USA are: the sugar pine (P. lambertiana), western white pine (P. monticola), eastern white pine (P. strobus). In China the most susceptible are: the Chinese red pine (P. massoniana) and the armandi pine (P. armandii) (Chen, 2004).
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Fungi
- Phylum: Basidiomycota
- Subphylum: Pucciniomycotina
- Class: Pucciniomycetes
- Order: Pucciniales
- Family: Cronartiaceae
- Genus: Cronartium
- Species: Cronartium ribicola
Notes on Taxonomy and NomenclatureTop of page The specific forms f.sp. ribicola and f.sp. pedicularis have been proposed to indicate infectability of different hosts. However, f.sp. pedicularis can infect both Ribes and Pedicularis (Yokota and Uozumi, 1976; Shi, 1991). Successful inoculations of Castilleja miniata using aeciospores from infected pines were obtained by Hiratsuka and Maruyama (1976) and Patton and Spear (1989). The latter also infected Pedicularis resupinata and P. canadensis, and Phaseolus vulgaris. However, Hunt (1984) did not obtain infection (visible to the eye) of Castilleja hispida or C. miniata, Pedicularis species or Rhinanthus crista-galli. Hunt (1984) and Patton and Spear (1989), inoculated Ribes species successfully. Hiratsuka and Maruyama (1976) reported telia on Castilleja stems, whereas Patton and Spear (1989) found extensive mycelia in leaves, but no spore production from any Castilleja, Pedicularis or Phaseolus plants. Yi and Kim (1983) successfully inoculated native Pedicularis and Ribes montigenum from Pinus koraensis, but not R. nigrum or R. grossularia [R. uva-crispa] or two native Ribes species. Kovaleva and Natal'ina (1968) determined that two 'forms' of C. ribicola existed due to spore morphology and reported the incapacity of spores from currant to infect gooseberry. Therefore, 'specialized' C. ribicola populations may exist, but apparently not to the degree of separation needed to qualify as formae speciales.
There are some indications that geographic speciation is currently taking place. Genetic drift in eastern and western populations of North America and restriction in gene flow are possible mechanisms of geographic speciation. Recent spread and intensification in new hosts or geographic regions, e.g., in the southwest (P. strobiformis), at high elevation (P. albicaulis), and in eastern stands of limber pine (P. flexilis) could result in a genetic bridge between eastern and western C. ribicola (Hamelin, 2003).
DescriptionTop of page After Laundon and Rainbow (1971):
Heteroecious, macrocyclic. Pycnia caulicolous, appearing as low yellowish blisters towards the edge of the cankers, becoming irregular, ill defined and dark coloured, gradually destroyed or disrupted by the enlarging aecia, of indeterminate type, subcortical, flat, ca 50 µm deep and 0.5-3 mm diameter. Aecia caulicolous, peridermioid, more or less circular and ca 2-5 mm diameter or transversely elongated and up to 10 x 5 mm, opening irregularly or around the sides; peridia smooth, several cells thick; cells elongated, strongly verrucose. Aeciospores globose to ellipsoid, 16-30 µm diameter (20-34 x 13-25 µm on Pinus pumila; Imazu and Kakashima, 1995); wall hyaline, 2-4.5 µm thick, often slightly thicker at the smooth spot than around rest of the spore, strongly verrucose, except for the well-defined smooth spot, the warts 1-2 µm diameter x 1-2 µm high. Uredinia hypophyllous, on angular brownish or dark spots, often profuse, yellowish, bullate, circular, minute, 0.15-0.25 mm diameter, peridiate with a central pore. Urediniospores ellipsoid to obovoid, 19-30 x 13-20 µm (21-32 x 13-22 µm on Pinus pumila; Imazu and Kakashima, 1995); wall hyaline, 1-2 µm thick, finely echinulate with spines 2-3 µm apart x 1 µm high, pores apparently absent. Telia appearing in the uredinia and producing spore columns up to 2 mm long and 0.1-0.2 mm wide, orange to cinnamon brown, often profuse and like a coarse felt on the leaf undersurface. Teliospores somewhat cemented together, ellipsoid at apex of the telial columns, cylindric below, rounded or truncate ends, 28-60 x 15-23 µm; wall hyaline, pale yellowish to golden, 1-2 µm thick, often thickened at ends or corners to 4-6 µm, smooth. The Aeciospores measure 14.4-28.8x22.8-33.6 µm and Urediospores measure 13.1-20.6x15.6-30 µm (Chen, 2004).
DistributionTop of page The rust is found in a circumpolar belt in the northern hemisphere wherever susceptible hosts occur within range of spores from the other. Aeciospores seem more durable than other spores and may account for most reports of infected Ribes beyond the range of susceptible pines.
The distribution table contains details of specimens held in herb. IMI (CABI, Egham, UK).
Distribution TableTop 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/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|China||Restricted distribution||Cheng et al., 1998a; IMI Herbarium, unda; Tai, 1979; Song, 1988; Guo, 1989; CABI/EPPO, 2000; EPPO, 2014|
|-Gansu||Present||Jing et al., 1995; CABI/EPPO, 2000; EPPO, 2014|
|-Heilongjiang||Present||Cheng et al., 1995; CABI/EPPO, 2000; EPPO, 2014|
|-Jilin||Present||Shao et al., 1980; Cheng et al., 1995; CABI/EPPO, 2000; EPPO, 2014|
|-Liaoning||Present||Cheng et al., 1995; CABI/EPPO, 2000; EPPO, 2014|
|-Shaanxi||Present||Jing et al., 1995; CABI/EPPO, 2000; EPPO, 2014|
|-Sichuan||Present||Native||Sawada, 1942; Yang, 2002; Chen, 2004|
|-Xinjiang||Present||Jing et al., 1995; Yao et al., 1995; CABI/EPPO, 2000; EPPO, 2014|
|-Yunnan||Present||Chen et al., 2006|
|India||Restricted distribution||Anon., 1961; IMI Herbarium, unda; Arthur and Cummins, 1933; CABI/EPPO, 2000; EPPO, 2014|
|-Jammu and Kashmir||Present||CABI/EPPO, 2000; EPPO, 2014|
|Iran||Present||Khabiri, 1962; CABI/EPPO, 2000; EPPO, 2014|
|Japan||Present||Wicker & Yokota, 1976; Saho, 1972; Hobayashi, 1976; Yokota and Uozumi, 1976; Hiratsuka et al., 1992; CABI/EPPO, 2000; EPPO, 2014|
|-Hokkaido||Present||Imazu and Kakishima, 1995; CABI/EPPO, 2000; EPPO, 2014|
|-Honshu||Present||Hama, 1987; Imazu and Kakishima, 1995; CABI/EPPO, 2000; EPPO, 2014|
|Korea, DPR||Present||CABI/EPPO, 2000; EPPO, 2014|
|Korea, Republic of||Present||Hyun and Koo, 1981; Kim et al., 1982; Yi, 1982; Yi and Kim, 1983; La and Yi, 1995; CABI/EPPO, 2000; EPPO, 2014|
|Nepal||Present||Durrieu, 1980; Ono et al., 1990; CABI/EPPO, 2000; EPPO, 2014|
|Pakistan||Present||Ahmad, 1956; Zakaullaii, 1994; CABI/EPPO, 2000; EPPO, 2014|
|Taiwan||Present||Sawada, 1942; Anon., 1979; Hiratsuka and Chen, 1991; CABI/EPPO, 2000; EPPO, 2014|
|Canada||Widespread||IMI Herbarium, unda; Hiratsuka and Powell, 1976; Ginns, 1986; CABI/EPPO, 2000; Hilton, 2000; EPPO, 2014|
|-Alberta||Present||Smith, 1971; Ziller, 1974; CABI/EPPO, 2000; EPPO, 2014|
|-British Columbia||Present||Ziller, 1974; Wood, 1986; Allen et al., 1996; CABI/EPPO, 2000; Campbell and Antos, 2000; Zeglen, 2000; EPPO, 2014|
|-Manitoba||Present||Ginns, 1986; CABI/EPPO, 2000; EPPO, 2014|
|-New Brunswick||Present||Magasi, 1991; CABI/EPPO, 2000; EPPO, 2014|
|-Newfoundland and Labrador||Present||CABI/EPPO, 2000; EPPO, 2014|
|-Nova Scotia||Present||Magasi, 1991; CABI/EPPO, 2000; EPPO, 2014|
|-Ontario||Present||Bérube & Plourde, 1995; Zsuffa, 1985; Hodge et al., 1990; CABI/EPPO, 2000; EPPO, 2014|
|-Prince Edward Island||Present||Magasi, 1991; CABI/EPPO, 2000; EPPO, 2014|
|-Quebec||Present||Bérube & Plourde, 1995; Lavalée, 1974; Lavalée, 1986; Therrriault 1993; Corriveau and Lamontagne, 1977; CABI/EPPO, 2000; EPPO, 2014|
|-Saskatchewan||Present||Ginns, 1986; CABI/EPPO, 2000; EPPO, 2014|
|USA||Widespread||IMI Herbarium, unda; Anon., 1960; Boyce, 1961; Neuenschwander et al., 1999; CABI/EPPO, 2000; Smith and Hoffman, 2000; EPPO, 2014|
|-Arizona||Present||Fairweather and Geils, 2011; EPPO, 2014|
|-California||Present||Native||Byler & Parmeter, 1979; Miller, 1968; Kinloch and Comstock, 1981; Samman, 1982; Chen et al., 1985; Kliejunas, 1985; French, 1987; CABI/EPPO, 2000; Smith and Hoffman, 2000; Chen, 2004; EPPO, 2014|
|-Colorado||Present||CABI/EPPO, 2000; Hummer, 2000; Johnson and Jacobi, 2000; EPPO, 2014|
|-Connecticut||Present||CABI/EPPO, 2000; Frederick et al., 2011; EPPO, 2014|
|-Delaware||Present||Anon., 1960; CABI/EPPO, 2000; EPPO, 2014|
|-Georgia||Present||Hepting and Toole, 1950; CABI/EPPO, 2000; EPPO, 2014|
|-Idaho||Present||Krebill, 1964; Shaw, 1973; Bingham, 1983; Tomback et al., 1995; CABI/EPPO, 2000; Smith and Hoffman, 2000; EPPO, 2014|
|-Illinois||Present||CABI/EPPO, 2000; EPPO, 2014|
|-Indiana||Present||Emmons et al., 1960; CABI/EPPO, 2000; EPPO, 2014|
|-Iowa||Present||CABI/EPPO, 2000; EPPO, 2014|
|-Maine||Present||Ostrofsky el al., 1988; CABI/EPPO, 2000; EPPO, 2014|
|-Maryland||Present||CABI/EPPO, 2000; EPPO, 2014|
|-Massachusetts||Present||Miller, 1973; CABI/EPPO, 2000; EPPO, 2014|
|-Michigan||Present||van Ardsel & Krebill, 1995; King, 1958; Anderson, 1973; Robbins et al., 1988; CABI/EPPO, 2000; Ostry, 2000; EPPO, 2014|
|-Minnesota||Present||van Ardsel & Krebill, 1995; King, 1958; Anderson, 1973; CABI/EPPO, 2000; Ostry, 2000; EPPO, 2014|
|-Montana||Present||Brown, 1970; Shaw, 1973; CABI/EPPO, 2000; EPPO, 2014|
|-Nevada||Present||CABI/EPPO, 2000; Hummer, 2000; Smith and Hoffman, 2000; Smith et al., 2000; EPPO, 2014|
|-New Hampshire||Present||Miller, 1973; Lombard and Bofinger, 1999; CABI/EPPO, 2000; EPPO, 2014|
|-New Jersey||Present||Miller, 1973; CABI/EPPO, 2000; EPPO, 2014|
|-New Mexico||Present||Hawksworth, 1990; Conklin, 1994; van Ardsel et al., 1998; Geils et al., 1999; CABI/EPPO, 2000; EPPO, 2014|
|-New York||Present||Miller, 1973; CABI/EPPO, 2000; EPPO, 2014|
|-North Carolina||Present||Hepting and Toole, 1950; CABI/EPPO, 2000; EPPO, 2014|
|-North Dakota||Present||Draper and Walla, 1993; CABI/EPPO, 2000; EPPO, 2014|
|-Ohio||Present||CABI/EPPO, 2000; EPPO, 2014|
|-Oregon||Present||Shaw, 1973; Samman, 1982; McDonald et al., 1984; Sniezko, 1994; CABI/EPPO, 2000; EPPO, 2014|
|-Pennsylvania||Present||Miller, 1973; CABI/EPPO, 2000; EPPO, 2014|
|-Rhode Island||Present||Miller, 1973; CABI/EPPO, 2000; EPPO, 2014|
|-South Dakota||Present||Lundquist et al., 1992; CABI/EPPO, 2000; EPPO, 2014|
|-Tennessee||Present||CABI/EPPO, 2000; EPPO, 2014|
|-Utah||Present||CABI/EPPO, 2000; Smith and Hoffman, 2000; EPPO, 2014; Vogler et al., 2017|
|-Vermont||Present||Miller, 1973; Bergdahl and Teillon, 2000; CABI/EPPO, 2000; EPPO, 2014|
|-Virginia||Present||Stipes and Davis, 1972; CABI/EPPO, 2000; EPPO, 2014|
|-Washington||Present||Shaw, 1973; Samman, 1982; Sniezko, 1999; CABI/EPPO, 2000; EPPO, 2014|
|-West Virginia||Present||CABI/EPPO, 2000; EPPO, 2014|
|-Wisconsin||Present||Native||Van Ardsel & Krebill, 1995; King, 1958; Greene, 1960; Anderson, 1973; CABI/EPPO, 2000; Meier, 2000; Ostry, 2000; EPPO, 2014|
|-Wyoming||Present||Harris, 1999a; Harris, 1999b; Brown, 1978; Lundquist, 1993; CABI/EPPO, 2000; Smith and Hoffman, 2000; EPPO, 2014|
|Austria||Widespread||****||Glaeser, 1974; CABI/EPPO, 2000; EPPO, 2014|
|Belarus||Present||Darozhkin & Federau, 1976; Gryshanocivh, 1976; CABI/EPPO, 2000; EPPO, 2014|
|Belgium||Present||Spaulding, 1961; CABI/EPPO, 2000; EPPO, 2014|
|Czech Republic||Restricted distribution||****||Tubeuf, 1936; Jankovsky, 1998; CABI/EPPO, 2000; EPPO, 2014|
|Czechoslovakia (former)||Restricted distribution||****||IMI Herbarium, unda; Tubeuf, 1936|
|Denmark||Present||Peterson, 1978; Nielsen and Kirknel, 1986; CABI/EPPO, 2000; EPPO, 2014|
|Estonia||Present||Lepik, 1937; CABI/EPPO, 2000; EPPO, 2014|
|Finland||Widespread||IMI Herbarium, unda; Kari, 1957; Kurkela and Jalkanen, 1998; CABI/EPPO, 2000; EPPO, 2014|
|France||Widespread||IMI Herbarium, unda; Arnaud and Arnaud, 1931; Monnet, 1989; CABI/EPPO, 2000; EPPO, 2014|
|Germany||Present, few occurrences||****||IMI Herbarium, unda; Braun, 1982; Muller, 1989; CABI/EPPO, 2000; EPPO, 2014|
|Hungary||Restricted distribution||****||IMI Herbarium, unda; Szabo, 1998; CABI/EPPO, 2000; EPPO, 2014|
|Ireland||Widespread||McKay et al., 1951; CABI/EPPO, 2000; EPPO, 2014|
|Italy||Present||CABI/EPPO, 2000; EPPO, 2014|
|Latvia||Present||Anon., 1956; CABI/EPPO, 2000; EPPO, 2014|
|Lithuania||Present||Minkevicius & Ignataviciute, 1991; Brundza, 1961; CABI/EPPO, 2000; EPPO, 2014|
|Netherlands||Present||CABI/EPPO, 2000; EPPO, 2014|
|Norway||Restricted distribution||****||Jorstad & Gjaerum, 1964; CABI/EPPO, 2000; EPPO, 2014|
|Poland||Present||IMI Herbarium, unda; Tylus et al., 1981; Nowacka et al., 1990; CABI/EPPO, 2000; EPPO, 2014|
|Romania||Present||IMI Herbarium, unda; Blada, 1990; CABI/EPPO, 2000; EPPO, 2014|
|Russian Federation||Restricted distribution||Kuprevich and Transhel, 1957; Spaulding, 1961; Kuminova, 1980; CABI/EPPO, 2000; EPPO, 2014|
|-Central Russia||Present||CABI/EPPO, 2000; EPPO, 2014|
|-Eastern Siberia||Present||CABI/EPPO, 2000; EPPO, 2014|
|-Russian Far East||Present||Ablakatova, 1965; Kakishima et al., 1995; Gjaerum, 1996; Imazu et al., 1998; Azbukina, 2000; CABI/EPPO, 2000; EPPO, 2014|
|-Western Siberia||Present||EPPO, 2014|
|Slovakia||Present||Hrubik, 1972; CABI/EPPO, 2000; EPPO, 2014|
|Spain||Present||Torres, 1959; CABI/EPPO, 2000; EPPO, 2014|
|Sweden||Restricted distribution||****||IMI Herbarium, unda; Spaulding, 1961; CABI/EPPO, 2000; EPPO, 2014|
|Switzerland||Widespread||****||IMI Herbarium, unda; Darbellay, 1939; CABI/EPPO, 2000; EPPO, 2014|
|UK||Restricted distribution||****||IMI Herbarium, unda; Spaulding, 1961; CABI/EPPO, 2000; EPPO, 2014|
|-England and Wales||Restricted distribution||IMI Herbarium, unda; CABI/EPPO, 2000; EPPO, 2014|
|-Northern Ireland||Restricted distribution||CABI/EPPO, 2000; EPPO, 2014|
|-Scotland||Restricted distribution||CABI/EPPO, 2000; EPPO, 2014|
|Ukraine||Present||Sherengovyi, 1979; CABI/EPPO, 2000; EPPO, 2014|
|Yugoslavia (Serbia and Montenegro)||Present||CABI/EPPO, 2000|
History of Introduction and SpreadTop of page Accidentally introduced to North America in 1910, white pine blister rust has spread across the range of the five-needled white pines. All eight of the western North American species of white pines are susceptible to this pathogen. These pines occur in ecosystems from near sea level to the tree-line. Six of these eight species have already been affected, several severely. Prior to 2003 there were no known cases of bristlecone (Pinus aristata, P. longaeva) with blister rust infection in natural stands, but blister rust was known to occur dangerously close to both the ancient Great Basin bristlecone pines (P. longaeva) in California, USA, and the Rocky Mountain bristlecones (P. aristata) in Colorado, USA. In 2003, a Rocky Mountain bristlecone with infection was discovered (J Blodgett, USDA Forest Service, USA, personal communication, 2004).
Non-native invasive pathogens such as white pine blister rust (C. ribicola) are killing trees and disrupting forest ecosystems in western North America. Populations of western white pine (P. monticola), sugar pine (P. lambertiana), whitebark pine (P. albicaulis), and limber pine (P. flexilis) are declining precipitously from damage by blister rust (Sniezko et al., 2004).
Risk of IntroductionTop of page Ribes cultivation is banned in some states of the USA (McKay, 2000). Importation of Ribes plants to North America is banned (Dale, 2000). Phytosanitary certification is required for shipments between Canada and the USA of Ribes plants and foliage or seedlings of susceptible pines. West Virginia, USA, prohibits cultivation of Ribes nigrum throughout the State, and of any Ribes species in 23 named counties (Gibson, 2000). Quarantine and Ribes eradication laws also exist in Pennsylvania (Hall, 2000); in New York State Ribes cultivation is regulated (Denham, 2000). Quarantines against importing the rust are established in Turkey, Argentina, Chile, Uruguay and the USA (EPPO, 1999). Although not found in Macedonia, C. ribicola is listed as 'economically important' and a separation of 2 km is suggested for the planting of Ribes and susceptible pines (Pinus peuce and P. strobus) (Papazov et al., 2000).
Hosts/Species AffectedTop of page
The centre of origin of C. ribicola is believed to be central-eastern Eurasia with Ribes and Pedicularis as alternate hosts (Millar and Kinloch, 1991) and pines in the subsections Cembrae and Strobi as additional hosts (Little and Critchfield, 1969). The rust was found on pines and currants in Europe in the 1800s (Hummer, 2000). It was transported to eastern North America on infected pine seedlings in the late 1800s and to the west coast in 1910 (Hummer, 2000). Now it occurs throughout the range of susceptible hosts, including two species in subsection Balfourianae, and seems to be expanding southward on pines in western USA (Hawksworth, 1990). It occurs on Ribes beyond the range of susceptible pines (for example in Saskatchewan, Canada; Ginns, 1986).
In addition to the main hosts listed, C. ribicola has been reported by various researchers from another 14 species of Pinus species and over 40 other species of Ribes. In inoculation trials, C. ribicola formed uredinia or telia on seven species of Ribes, Pedicularis palustris subsp. palustris, Bartsia alpina and Loasa triphylla (Kaitera et al., 2012).
Host Plants and Other Plants AffectedTop of page
|Castilleja (paintbrushes)||Scrophulariaceae||Wild host|
|Castilleja miniata||Scrophulariaceae||Wild host|
|Pedicularis (lousewort)||Scrophulariaceae||Wild host|
|Pedicularis bracteosa||Pediculidae||Wild host|
|Pedicularis racemosa||Scrophulariaceae||Wild host|
|Pinus albicaulis (whitebark pine)||Pinaceae||Main|
|Pinus aristata (bristle-cone pine)||Pinaceae||Main|
|Pinus aristata var. longaeva||Pinaceae||Main|
|Pinus aristata var. longaeva||Pinaceae||Other|
|Pinus flexilis (limber pine)||Pinaceae||Other|
|Pinus koraiensis (fruit pine)||Pinaceae||Main|
|Pinus lambertiana (big pine)||Pinaceae||Main|
|Pinus monticola (western white pine)||Pinaceae||Main|
|Pinus parviflora (Japanese white pine)||Pinaceae||Main|
|Pinus parviflora var. pentaphylla||Pinaceae||Main|
|Pinus pumila (Dwarf Siberian pine)||Pinaceae||Main|
|Pinus strobus (eastern white pine)||Pinaceae||Main|
|Ribes alpinum (alpine current)||Grossulariaceae||Other|
|Ribes americanum (American black currant)||Grossulariaceae||Other|
|Ribes aureum (golden currant)||Grossulariaceae||Other|
|Ribes bracteosum (Stink currant)||Grossulariaceae||Other|
|Ribes cereum (Wax currant)||Grossulariaceae||Other|
|Ribes glandulosum (Skunk currant)||Grossulariaceae||Other|
|Ribes hirtellum (Hairystem gooseberry)||Grossulariaceae||Other|
|Ribes hudsonianum var. petiolare (Western black currant)||Grossulariaceae||Other|
|Ribes lacustre (Swamp black currant)||Grossulariaceae||Other|
|Ribes laxiflorum (Trailing black currant)||Grossulariaceae||Other|
|Ribes lobbii (Lobbs gooseberry)||Grossulariaceae||Other|
|Ribes montigenum (Mountain gooseberry)||Grossulariaceae||Other|
|Ribes nevadense (Sierra currant)||Grossulariaceae||Other|
|Ribes nigrum (blackcurrant)||Grossulariaceae||Main|
|Ribes oxyacanthoides (Northern gooseberry)||Grossulariaceae||Other|
|Ribes roezlii (Sierra gooseberry)||Grossulariaceae||Other|
|Ribes rubrum (red currant)||Grossulariaceae||Other|
|Ribes sanguineum (Flowering currant)||Grossulariaceae||Other|
|Ribes speciosum (Fuchsia-flowered gooseberry)||Grossulariaceae||Other|
|Ribes triste (Swamp red currant)||Grossulariaceae||Other|
|Ribes uva-crispa (gooseberry)||Grossulariaceae||Other|
Growth StagesTop of page Flowering stage, Fruiting stage, Seedling stage, Vegetative growing stage
SymptomsTop of page On Pines: 'flagged' branches (with dead foliage) or tops distal to swollen, rough-barked branches or stems producing resin flow from an orange-margined canker. Young trees may be stunted and discoloured prior to death. Younger cankers are elongated and spindle-shaped on branches and diamond-shaped on stems within the orange margin. Conspicuous, orange, aecia develop in spring, followed by oozing pycnia.
On Ribes: orange-yellow spots appear on leaves in early summer; mycelia are visible from the under surface. In late summer, leaves show more-developed spots and necrotic areas, and may be curled. Telial columns are visible to the eye in brownish spots on the under surface.
List of Symptoms/SignsTop of page
|Leaves / abnormal leaf fall|
|Leaves / necrotic areas|
|Leaves / wilting|
|Leaves / yellowed or dead|
|Stems / canker on woody stem|
|Stems / discoloration of bark|
|Stems / distortion|
|Stems / external feeding|
|Stems / gummosis or resinosis|
|Stems / ooze|
|Stems / visible frass|
|Whole plant / distortion; rosetting|
|Whole plant / dwarfing|
|Whole plant / external feeding|
|Whole plant / frass visible|
|Whole plant / plant dead; dieback|
Biology and EcologyTop of page Life Cycle
Peterson (1974) classified C. ribicola as macrocyclic since it produces five spore forms, which differ in the distribution of chitin on cell surfaces (Ekramoddoullah et al., 2000).
Inoculation of Pinus species by basidiospores generally requires cool temperatures (9-15°C; Hansen and Patton, 1975; Yokota, 1983b). Moist air is critical, but droplets on leaf surfaces can cause spore clumping and bursting (Hansen and Patton, 1977). Spore germination is affected by pH (Bega, 1960). Tube growth is directionless, but the tube must enter stomates and proliferate in the sub-stomatal chamber (Patton and Spear, 1978). Light to maintain open stomata may be helpful. Blockage of pine stomata by wax may be a 'defence mechanism' (Patton et al., 1980). Fungal hyphae may employ proteins to overcome defence responses (Ekramodoullah et al., 1999) or enzymes (pectinase) to break down cell walls and facilitate penetration (Martin, 1980) once hyphae are through the stoma. Infected pines express defence-responsive PR-10 genes (Yu et al., 2000). Catabolic effects in the host tissue several millimetres from mycelia produce tannins in the cytoplasm and vacuoles (Robb et al., 1975a, b). Changes may occur also in RNase (Harvey, 1979), and in cytokinins, Ca and K contents and glycine-2-C14 in the host (Lee, 1975).
Macro symptoms (needle spots) appear the following spring, or earlier in greenhouses. Extension to the bark, producing an orange spot at the base of a leaf cluster, may occur the same year. Mycelia may be found in the bark up to 12 cm beyond the orange band (Harvey and Cohen, 1958). Pycnia may emerge from inside the orange margin of the swelling canker the first or second year following infection reaching the bark. Insects, slugs and squirrels are attracted to pycnia (Powell, 1982; Hunt, 1985); the fluid contains many sugars, including high concentrations of glucitol and ribitol (Wicker et al., 1976). Insects may effect cross-transfer of genetic material (Hunt, 1985), producing multi-genotype cankers (McDonald, 1978; Hamelin, 1996). Hardy-Weinberg equilibrium of alleles in basidiospores implies random transfer of genetic material among pycnia (Gitzendanner et al., 1996).
Aeciospores develop the second or subsequent years after infection and spread to alternate hosts in the spring. 'Dormant' Ribes buds may be more susceptible than expanding leaves (Harvey, 1972). Infected Ribes leaves develop chlorotic spots that produce urediniospores from late spring to late summer, leading to increased and intensified infection by cycles of urediniospores. Telial columns develop by early summer to late autumn. Haploid basidiospores are produced during that time, infecting susceptible pines under favourable conditions: usually cool, moist air with gentle winds in late summer to early autumn. However, more-successful early-season infection has been found (Hunt and Jensen, 2000). Spaulding (1922) found viable spores shed into late autumn.
The fungus overwinters as hyphae from new infections in intact pine foliage and in bark from established infections. The infection on Ribes ends with leaf drop. Temperature and moisture are both important to rust spread (van Ardsel et al., 1956; van Ardsel, 1965b). Spore spread from pine occurs in spring via aeciospore release on wind, matching a linear prediction (Burleigh et al., 1978). Although aeciospores can travel several kilometres, unlike basidiospores (Buller, 1950), spread of a new virulent rust allele vs. sugar pine has been slow (Kinloch and Dupper, 1987) and seems vulnerable to loss via genetic drift (Kinloch et al., 1998a). Intensification of an outbreak depends on the local climate (Song, 1988; van Ardsel and Krebill, 1995) and the distribution, density and susceptibility of the alternate hosts (Kim et al., 1982). Differences in Ribes susceptibility have been documented (McDonald and Andrews, 1981; Maloy, 1997). Pines generally differ in susceptibility relative to their proximity to the apparent centre of rust origin: Asiatic species are generally the least susceptible, European species more so, and North American species the most susceptible (Bingham, 1972). A similar trend exists in European vs. North American species of Ribes (Maloy, 1997).
Some reduction in aeciospore production may result from feeding by slugs (Hunt, 1978), and mice, squirrels, hares and porcupines (Powell, 1982). Several fungi are associated with C. ribicola cankers on pines (Williams, 1972). The associated fungus Tuberculina maxima, which capitalizes on tissue invaded by C. ribicola (Wicker and Woo, 1973), has been found with inactive rust cankers on Pinus monticola (Kimmey, 1969; Hungerford, 1977; Wicker, 1981), but not in Japan (Wicker and Yokota, 1982). T. maxima showed no evidence of antibiosis, lysis or parasitism of C. ribicola in a co-culture trial (Wicker, 1979). Its biocontrol potential seems limited (Wicker et al., 1980).
'High' infection caused Ribes mortality in a study by Mielke (1937) in British Columbia, Canada. Merrill (1991) summarized rust-intensification rates for several outbreaks in North America. The trend of rate of increase per unit per year was logarithmic at low disease incidence, but logistic at high levels. A model of rust epidemics has been created (MacDonald et al., 1981).
C. ribicola, introduced to Minnesota, USA, around 1914, is the cause of a decline in the eastern white pine (Pinus strobus) population of the north-east of that state over the past 100 years. Along with other factors, such as herbivore browsing, C. ribicola now poses a major challenge to the reestablishment of white pines in the region. White pine regeneration may be possible with modern geographical information system techniques and readily available spatial databases, which show that climate, topographic characteristics, distances from water bodies and wetlands have had a strong influence on the white pine blister rust infection hazard (White et al., 2002).
A major survey of white bark pines (P. albicaulis) was conducted throughout its range in British Columbia, Canada. Over 3 years, 24,070 trees were examined for cause of death. Thirty-one percent had active blister rust infections. Finding relationships between the proportion of healthy, infected, or dead trees and elevation, latitude, and longitude produced mixed results. Rust infection occurred 4% of the time in larger trees (Zeglen, 2002).
In northern Wisconsin, USA, a survey showed the topographic position, aspect, slope, tree density, habitat type, and the presence or absence of bole cankers, at each plot. The mean incidence of infection was 7.2%. Mean incidence of canker-infected trees at this site was 15.9%. Incidence was almost three times higher on ridge tops and shoulders (12.3%) than on flat or bottomland (4.7%). The mean incidence of infection was 7.2% for all study sites, and 5.9% excluding data from Bayfield Peninsula. Incidences were almost three times higher on ridge tops and shoulders (12.3%) than on flat or bottomland (4.7%). Habitat type was correlated with disease incidence only at the Bayfield Peninsula site, and slope was not significantly correlated with rust levels on any of the plots (Dahir and Carlson, 2001).
Information about effects of plant spacing on growth and development of western white pine (P. monticola) is scant, because C. ribicola has severely limited the survival of trees in young plantations. The plots were measured again at ages 11 and 16. 16 years after planting, survival averaged 80%. 71% of the planted trees were free of blister rust at age 16. We believe that rust-resistant stock of western white pine merits greater consideration for planting in the Douglas-fir region. (Bishaw et al., 2003).
C. ribicola has been found on P. armandii (alternate host: Ribes glaciale var. laciniatum) in Sichuan, China. It was a localized, serious epidemic rust in the south and south-west and also in the Himalayas of China (Chen, 2004, Yang ZZ, 2002).
In China, the Chinese five needles pine blister rust attacks the Chinese red pine (P. koraiensis), the alternate hosts are Ribes and Pedicularis (Chen, 2004).
Genetic variation in C. ribicola has been inferred from sudden increases in pine infection in the USA (Kinloch and Comstock, 1981; McDonald et al., 1984) and in Pakistan (Zakaullaii, 1994). Differences in pine infection developed in trials using different rust sources (Stephan and Hyun, 1983; Meagher and Hunt, 1999). Differences in spore germination between Idaho and California collections may indicate ecotypes adapted to those environments (McDonald, 1996).
Intra-population variation in rust, causing different spot colours on a tree, have been found (McDonald and Hoff, 1972). Such studies are summarized to 1992 by Hoff and McDonald (1993). More recent work has employed isoenzyme, RAPD and RFLP techniques, and DNA mapping (White et al., 1996; Cheng et al., 1998b; Kinloch et al., 1998b, 1999). Uniformity in rust from north-east China suggested its recent arrival (Cheng et al., 1998a). In North America, studies have found much intra-population variation, but no clear geographic pattern (Bérube and Plourde, 1995; Hamelin et al., 1995, 1998). Different genotypes (Hamelin, 1996) or ribosomal intergenic spacer lengths (White et al., 1996) were found in a single canker. Rusts from eastern vs. western North America may show little genetic differentiation (Kinloch et al., 1998b) or clear differences (Hamelin et al., 1998). Cytoplasmic control of a gene virulent to a single defence gene in Pinus lambertiana is reported (Kinloch and Dupper, 1999).
A gene 'Cr' has been found in Ribes nigrum that resists C. ribicola (Ogol'tsova, 1979). This gene, dominant in Ribes ussuriense, conferred immunity to R. nigrum cultivars against North American strains of blister rust (Zambino, 2000).
Relatively high levels of blister rust infection (caused by C. ribicola) in some stands of genetically improved western white pine (P. monticola) raised concerns that resistance may fail under field conditions. Surveys show that infection and mortality are consistently lower in genetically improved white pine as compared to unimproved stock. In order to restore white pine populations and help alleviate forest health problems in the Inland Northwest forests of the USA, it is recommended that breeding for high levels of rust resistance continues, and planting of resistant seedlings increases, along with other silvicultural treatments (Fin et al., 2002).
The antigen reaction to an anti mab 7 suggests a constitutive role for Cro r II in fungus as an antibody in engineered C. ribicola-resistant white pines (Yu, Xueshu et al., 2002).
Hypersensitive reactions (HR) were observed in south-western white pines (P. strobiformis), as it was previously in sugar pine (P. lambertiana, Cr1) and western white pine (P. monticola, Cr2), at frequencies ranging from very low to moderate, which indicates a single dominant allele for resistance (Cr3). HR was present at a relatively high frequency (19%). HR was not found in whitebark pine (P. albicaulis), Mexican white pine (P. ayacahuite), foxtail pine (P. balfouriana), or Great Basin bristlecone pine (P. longaeva). A very important point is made by Kinloch et al. (2002): "Although blister rust traditionally is considered an exotic disease in North America, these results, typical of classic gene-for-gene interactions, suggest that genetic memory of similar encounters in past epochs has been retained in this pathosystem". Chen (2004) wrote: "Although it has been suggested that white pine blister rust is introduced from outside of [the USA] in a portion of its current range, the occurrence of white pine blister rust floras in virgin forests indicates the WPBR has evolved as part of the indigenous ecosystem in each region".
The interaction of resistance and virulence in C. ribicola suggests that some populations are locally adapted. Knowledge of population genetic structure and host specialization will be useful for host resistance screening, gene deployment, and predicting pathogen adoption (Richardson, 2003).
The black currant clone, 'Farleigh,' was susceptible to C. ribicola, which occurred every year. 'Titania' and 'Intercontinental' had the best field resistance to diseases. (Pedersen, 2001). Ribes clones, treated for developed infection, showed Blackcurrant cultivars with the Cr gene for white pine blister rust-immune genotypes (Hummer et al., 2002).
'Ben Alder' was the most affected by the disease with 63% of the underleaf surface covered with uredinia by mid-August, a few days following harvest. 'Ben Lomond' showed an intermediate susceptibility with 24% of the leaves affected. 'Ben Nevis' and 'Ben Sarek' expressed a high level of resistance with only 5% of the leaves affected. 'Titania' was rust resistant (Rousseau et al., 2001).
Two new black currant cultivars, 'Tiben' (from 'Titania' crossed with 'Ben Nevis') and 'Tisel' (from self-pollination of 'Titania') are resistant to C. ribicola (Pluta et al., 2002).
Notes on Natural EnemiesTop of page On pines, feeding on cankers has been recorded by Powell (1982) and ascribed to chipmunks, porcupines and squirrels. Following observations of chewed cankers on infected Pinus strobus, feeding trials of red-backed vole (Clethrionomys andersoni) in Hokkaido, Japan, showed a preference for materials containing infected pine shoots or rust aeciospores (Maeda and Uozumi, 1981). Hunt (1978) reported feeding by slugs on the pycnial area of pine cankers. The main effect of this feeding was to reduce spore production, possibly slowing rust intensification. Insects attracted to pycnia may be feeders and may create heterothallic cankers by transfer of Cronartium genes (Hunt, 1985).
Means of Movement and DispersalTop of page Long-distance transfer of aeciospores seems responsible for reports of infection well beyond the range of susceptible pine species (Boyce, 1961; Smith, 1971; Ginns, 1986). Aeciospores are more durable and less-responsive to drying and heat shock than urediniospores and teliospores (Zambino et al., 1997) although urediniospores are fairly durable (Spaulding and Rathbun-Gravatt, 1925). Basidiospores are more susceptible to drying and solar damage (Spaulding, 1926). Night breezes are important in transferring basidiospores under conditions favouring inoculation (van Ardsel, 1965a).
Pathway VectorsTop of page
Plant TradeTop of page
|Plant parts liable to carry the pest in trade/transport||Pest stages||Borne internally||Borne externally||Visibility of pest or symptoms|
|Bark||hyphae; spores||Yes||Pest or symptoms usually invisible|
|Leaves||hyphae; spores||Yes||Yes||Pest or symptoms not visible to the naked eye but usually visible under light microscope|
|Seedlings/Micropropagated plants||hyphae; spores||Yes||Pest or symptoms usually invisible|
|Stems (above ground)/Shoots/Trunks/Branches||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|
|Fruits (inc. pods)|
|Growing medium accompanying plants|
|True seeds (inc. grain)|
ImpactTop of page The identification of C. ribicola as the same rust as that infecting cultivated Ribes virtually eliminated cultivation of Pinus strobus in Europe after 150 years (Laundon and Rainbow, 1971). In North America, its impact on all susceptible pine species has been severe The identification of C. ribicola as the same rust as that infecting cultivated Ribes virtually eliminated cultivation of Pinus strobus in Europe after 150 years (Laundon and Rainbow, 1971). In North America, its impact on all susceptible pine species has been severe (Boyce, 1961; Kliejunas, 1985; Hummer, 2000; Smith and Hoffman, 2000). Bega and Scharpf (1993) declared that white pine blister rust caused more damage and cost more to control than any other conifer disease in North America. The epidemic on Pinus monticola (Neuenschwander et al., 1999) was described as 'the world's most spectacular epiphytotic' (Bingham, 1983), causing a reduction of the gene pool of P. monticola (Hunt et al., 1985) and decimating regeneration of the threatened P. albicaulis (Tomback et al., 1995). However, Harvey (1967) found that branch cankers on P. lambertiana grew slower and died earlier, creating a lesser threat to survival, than similar cankers on P. monticola. Its impact on P. albicaulis and P. strobiformis is under recent study (Brown, 1978; Keane and Arno, 1993; Smith and Hoffman, 1998; Campbell and Antos, 2000; Zeglen, 2000). However, in mid-1980s C. ribicola caused trunk cankers in a sugar pine (P. lambertiana) plantation in the mid-Sierra Nevada mountains, killing 95% of the total number of trees (Chen, 2004). Susceptible Ribes species, especially R. nigrum, suffer reduced vigour and fruit yields.
Environmental ImpactTop of page As the white pines of the western USA are killed, the associated ecosystems also decline, altering the forest landscapes. In addition, these white pines are all moderately to greatly fire dependent, and have declined from past fire exclusion policies and the resulting successional replacement (Sniezko et al., 2004).
Impact: BiodiversityTop of page East Asia and North America were seriously attacked by C. ribicola during the 20th century, especially the western USA. There are nine white pine species native to the USA that are at risk and these include some of the oldest, and ecologically or culturally significant pine species in the USA. C. ribicola threatens the stability and survival of white pine ecosystems in 40 states of the USA. Without white pines, these forest communities would be altered dramatically (USDA-FS, 2004).
Threatened SpeciesTop of page
|Threatened Species||Conservation Status||Where Threatened||Mechanism||References||Notes|
|Pinus albicaulis (whitebark pine)||EN (IUCN red list: Endangered) EN (IUCN red list: Endangered); USA ESA candidate species USA ESA candidate species||California; Montana; Oregon; Wyoming||Pathogenic||US Fish and Wildlife Service, 2014|
Risk and Impact FactorsTop of page Impact mechanisms
DiagnosisTop of page Spore morphology can separate C. ribicola from C. occidentale (Colley, 1925; Colley et al., 1927), and from C. quercuum (Liu and Teng, 1986; Cheng et al., 1998b), but not according to Kasanen (1997). Randomly amplified polymorphic DNA (Cheng et al., 1998b) and monoclonal antibodies (Ekramoddoullah and Taylor, 1996) have been identified; the latter confirm C. ribicola in infected pines (Ekramoddoullah and Tan, 1998).
Recently, during the molecular analysis of the proteins and genes involved in the host-pathogen interaction, the C. ribicola fungal protein Cro rI was identified in infected white pine tissues. The C. ribicola genome contained at least two copies of the cro rI gene. The translocation of Cro rI was only found to occur in cankered trees, and not in the young infected seedlings. The implications of Cro rI in pathogenesis are discussed by Yu et al. (2002).
Detection and InspectionTop of page Pines: examine plants for spotted second-year or older foliage, swollen branches or stems inside an orange margin, pycnial ooze or orange aecial structures in a spindle-shaped swelling. Trees show dying branches or tops distal to cankers; stems may be greatly enlarged above the canker and cankers may produce heavy resinosis (Hoff, 1992; Hunt and Meagher, 1992).
Ribes: leaves show yellow-brown spots above and mycelia or brownish telial columns below. Leaves may curl conspicuously and drop early.
Similarities to Other Species/ConditionsTop of page On Pinus monticola, Atropellis pinicola forms cankers on branches. They differ from C. ribicola cankers in being flattened and not cracked through aecial production, but show darkened circular cups from the fruiting bodies. Wood under the cankers is stained black; C. ribicola causes no staining (Hunt and Meagher, 1992).
Prevention and ControlTop of page Introduction
Where the alternate hosts exist, control is necessary. Control measures differ to protect the most-important hosts.
Genetic resistance and species selection can be used as a means to control some rusts, and infected branches can be eliminated by pruning. Site hazard ratings based on habitat type and elevation are available. Ongoing research is evaluating ways to manage rust diseases in ways that maximize their benefit to forest ecosystems while limiting their detrimental effects on forest resources (Parks and Flanagan, 2001).
Because resistant individuals in all these species are rare, genetic variation may be reduced to the point where future populations may not be viable without active management (Sniezko, 2004).
Understanding host-pathogen interactions is important in managing yield loss and can aid in the identification of disease-resistant trees. Several resistance mechanisms to C. ribicola have been identified in pine. At the molecular level, several defence responsive proteins and their genes have been characterized. Some of these are identified to be potential candidates for markers associated with resistance or susceptibility (Ekramoddoullah and Hunt, 2002).
Programmes of screening and genetic improvement of pines are active in Canada (Corriveau and Lamontagne, 1977; Meagher and Hunt, 1985; Zsuffa, 1985; Hunt, 1999), the USA (Miller,1973; Hoff and McDonald, 1980; Murphy, 1982; Samman, 1982; Franc, 1988; Eramian, 1999; Kitzmiller and Samman, 1999; Sniezko, 1999; Meier, 2000), Romania (Blada, 1994) and Korea (Hyun and Koo, 1981). Field testing of second-generation Pinus monticola seedlings has begun (McDonald et al., 1994). North American trials of species from Asia and Europe indicated potential gain in rust resistance (Heimburger, 1972), but eventual problems with adaptation to climatic differences. Rust resistance generally was higher in species closer to the Asian centre of the rust and least in North American species (Bingham, 1972), whether conducted in Europe (Søegaard, 1972) or North America (Bingham, 1972). Most activity now is in North America, mainly in P. strobus, P. monticola and P. lambertiana.
Heritability and gain estimates have been developed: for example, "spots only" (McDonald and Hoff, 1971), reduced needle-lesion frequency (Meagher and Hunt, 1996), leaf shed (of infected leaves) (Hoff and McDonald, 1971), bark reaction (Hoff, 1986b), and tolerance (Hoff, 1986a; Hunt, 1997) in Pinus monticola. Rust-resistance heritability estimates have been determined for Pinus wallichiana in Romania (Blada, 1994). Dominant genes stopping rust in pine foliage are identified (Kinloch et al., 1999; Kinloch, 2000) and a linkage map is constructed to facilitate cloning (Harkins et al., 1998). Laboratory techniques have identified a protein associated with defence in pines (Ekramoddoullah et al., 1998), and cloned a resistance gene analogue (Kim and Brunsfeld, 2000). Peptides with a potential for use in genetic engineering have affected spore germination and morphology (Jacobi et al., 2000; Rioux et al., 2000).
The aim of the pine genetic improvement programmes is generally to reduce the impact of the disease so that commercially-useful wood can be obtained without exerting such selective pressure on the rust's gene pool that would increase the frequency of rare alleles (Samman, 1982; Meagher and Hunt, 1985).
Ribes hybrids and cultivars are being screened in Russia (Ravkin and Litvinova, 1976), Siberia (Kuminova, 1980), Ukraine (Sherengovyi, 1979), Slovakia (Kozmenko and Invanicka, 1994), Poland (Tylus et al., 1981; Zurawicz et al., 1996; Pluta and Broniarek-Niemiec, 2000), Denmark (Pedersen, 1998) and the USA (Keep et al., 1975; Hummer, 1997; Dorrance and Bergdahl, 1990). Some estimates of genetic resistance are determined for R. nigrum in Poland (Pluta et al., 1993, Zurawicz et al., 1996). Canada has produced immune and highly-resistant clones that produced too little fruit (Luffman, 2000).
Picton (2002) has used marker-assisted selection to screen cultivated or wild currants for rust-immunity. Ribes improvement programmes usually combine rust resistance with resistance to other pests, such as powdery mildew and leaf spot (Zurawicz et al., 1996; Dale, 2000). During the last half of the 20th century, development of genetic resistance superseded other direct control measures such as, Ribes spp. eradication and antibiotics, which proved either ineffective or unfeasible, in large areas of the white pine range (Kinloch, 2003a).
The distribution and frequency of the Cr2 gene for resistance to C. ribicola in western white pine (P. monticola) was surveyed in natural populations of the host. Because Cr2 is dominant and results in a conspicuous hypersensitive reaction (HR) in pine needles, the phenotype can readily be detected in offspring of susceptible seed parents fertilized by unknown Cr2 donors in the ambient pollen cloud. The diminishing frequency of Cr2 from the southern and central Sierra Nevada, USA, northward mirrors that of Cr1 in sugar pine (P. lambertiana) and points to this region as the origin of both genes (Kinloch, 2003b).
Cultural Control and Sanitary Methods
Eradication of Ribes to reduce infection of pines has been successful in some cases (van Ardsel, 1980; Ostrofsky et al., 1988), but not in Pennsylvania, USA (Hall, 2000), and generally not in the Pinus monticola zone, where there are more native species of Ribes (Toko et al., 1967; Carlson, 1978; Maloy et al., 1994; Maloy, 1997). Europe mainly eliminated cultivation of susceptible pines to protect the more-valuable Ribes fruit crops (Laundon and Rainbow, 1971), whereas some US states banned Ribes cultivation to protect pines (McKay, 2000). Pruning and scribing stem cankers in pine stands can reduce rust successfully if started early (Hungerford et al., 1982; Lehrer, 1982; Lavallée, 1991; Schwandt et al., 1994; Hunt, 1998), although thinning of pines can increase rust by facilitating spore travel (Hunt, 1998). Integration of Ribes control and other options have been developed (Hagle et al., 1989). Silvicultural control of rust on pines is outlined by Yi (1982).
Analysis of rust presence and severity has permitted the definition of hazard zones (Hunt, 1983; Lavallée, 1986) to aid allocation of the most-suited pine stock (Goddard et al., 1985) because predictions of field performance of improved stock have been incorrect in some cases (Hunt and Meagher, 1989; Hunt, 1994). Integrated control using the most-appropriate resistance level is being developed (McDonald, 1979). Model-based predictions of rust hazard and pine stock type have been developed (Rust, 1988; Geils et al., 1999).
Labour-intensive efforts were conducted in the Rocky Mountains, USA, to restore the habitat of whitebark pine (P. albicaulis) by using controlled burning and silvicultural treatments. These measures were used to counteract forest decline due to C. ribicola, and a native mountain pine beetle (Dendroctonus ponderosae) (Keane, 2001).
Hunt (2002) experimented with solid deer protectors to prevent blister rust from attacking white pines, and found that rust prevention using barriers is promising and warrants further testing.
Application of pesticides to pines is limited by logistics in rough terrain and the difficulty in hitting all the foliage or cankers on tall trees, plus irregular absorption due to moisture on the target, etc. (Maloy, 1997). Stem application of cycloheximide entails bark removal before spraying (Moss, 1957) and may result in only reducing spore production (Powers and Steagall, 1965). Aerial sprays of phytoactin were employed on Pinus monticola stands, but the results were difficult to assess (Dimond, 1966) and the programme was cancelled (Benedict, 1966; Maloy, 1997). Spraying triadimefon on pine seedlings in a nursery can give protection in plantations (Bérube, 1996). Fungal sprays to protect pine seedlings and to reduce C. ribicola on Ribes are being tested (Johnson et al., 1992; Bérube et al., 1998).
Ribes crops are protected by sprays in Denmark (Nielsen and Kirknel, 1986), Norway (Gjaerum and Langnes, 1984), Netherlands (Wilson, 1978), Germany (Bomeke, 1972), Poland (Mrozowska et al., 1973; Profic-Alwasiak et al., 1973; Nowacka et al., 1990; Cimanowski et al., 1995) and Romania (Vonica and Minoiu, 1977), but not in British Columbia, Canada (Anon., 1998).
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