Crumenulopsis pine dieback -Crumenulopsis sororia

Crumenulopsis sororia is an apothecia-forming ascomycete that causes cankers in the bark and wood of Pinus species in Europe. Its presence in North America is unlikely (Groves, 1969), but it is known to infect some native species and some introduced species, so that it may be considered a potential invader of North America, as well as other continents where northern pines are grown. Once introduced, its small size, resemblance to related canker-causing species, and spread by airborne spores would make control difficult.

Crumenulopsis sororia (P. Karst.) J.W. Groves 1969 (Ascomycetes, Helotiales)

Alternate State (Anamorph): Digitosporium piniphilum Gremmen

Apothecia appearing stalkless, emerging from cracked bark, often in clusters, cup- to saucer-shaped, dark brown to black, the exterior rough, somewhat hairy, inrolled when dry, interior disk (exposed when damp) pale, 2 mm diam.

Asci unitunicate, 100-120 (90-125) x 12-13 um, 8-spored.

Ascospores roughly in two columns (biseriate), hyaline, elongate-fusiform, occasionally 1-septate, 18-21 (-27) x 3-5 um. Paraphyses filiform, sometimes branched, tips to 3 um wide. (Dennis, 1978).

Host range: Various species of Pinus.

Geographic distribution: Groves (1969) discounted collection records of both of his Crumenulopsis species on pine in the USA, considering reports to represent observations of Atropellis species instead. Lack of reports of C. sororia from other countries with temperate climates may be due, likewise, to the difficulty of distinguishing it from related fungi.

Notes: Groves (1969) identifies an ectal excipulum of the apothecium, composed of thick-walled dark cells forming a textura angularis distinct from the textura intricata of the medullary excipulum. van Vloten and Gremmen (1953) describe the apothecium with marginal hairs to 100 um long, hymenium yellow-green, stipes 300-600 um and spores ellipsoidal, 12.9-30.1 x 5.7 um, 1-4-celled. Septation in ascospores appears to increase with age, since Hayes (1975) reports that it occurs after spore release.

The asexual form (Digitosporium piniphilum) produces pale brown conidia composed of multiple and unequal multicellular branches, resembling the fingers of a hand, in single or clustered cavities of dark pycnidia in the surface layer of bark (Sutton, 1980). On malt agar, the slow-growing mycelium is grayish to olive-green, producing a black pigment into the medium (Gremmen, 1959). Pycnidia are readily produced in culture on 2.5% malt agar (Batko and Pawsey, 1964). Hayes and Manap (1975) did not report pycnidia but described colonies on 2.5% malt agar as pale to smoke grey, becoming darker at the umbonate center, with margins appressed, even to irregular, exudates vinaceous-brown to fuscous, reverse blackish, with some isolates producing brownish to black pigment into agar. Optimum growth occurred at 15-22.5 C, usually faster in the dark.

Karsten described this fungus as a species of Crumenula in 1871, but transferred it to the subgenus Heteropeziza of Godronia when he synonymized Crumenula with Godronia in 1885. Rehm kept the species (with C. pinicola) in Crumenula de Not., but his concept of the genus is not accepted (Groves, 1969).

Nannfeldt combined the genus with Godronia and Durandia in the genus Scleroderris (Fr.) de Not. Ettlinger objected and retained four species in Crumenula. Seaver chose to follow Karsten in placing C. soraria and C. pinicola in Godronia (van Vloten and Gremmen, 1953).

Nevertheless, considering Ettlingers concept, Gremmen found that the four species differ in the structure of the apothecium. The excipulum of C. sororia and C. pinicola is composed of textura intricata and bears marginal hairs, rather than textura prismatica and marginal scales as in Crumenula abietina and C.laricina. Imperfect forms, where known, are also different. Provisionally keeping C. sororia and C. pinicola in Crumenula de Not., Gremmen placed the other two species in Scleroderris (van Vloten and Gremmen, 1953).

Groves (1969) noting nomenclatural difficulties with the status of the genus Crumenula, chose to create the new genus Crumenulopsis for C. soraria and C. pinicola, with the latter as type species.

SIMILARITIES TO OTHER SPECIES

In the related genus Cenangium Fries, some species of which occur on pine as saprobes,or weak parasites, the ascospores are ellipsoid. In Gremmeniella Morelet, the ascospores are multi-septate.

Cenangium ferruginosum Fr. ex Fr. is difficult to distinguish from C. sororia until mature apothecia are present (van Vloten and Gremmen, 1953). These lack a stipe and have neither hairs nor scales on the margin. Ascospores are ovate-ellipsoid, hyaline, aseptate, 12-13 X 5-6 Um. In culture, this species produces black spermagonia containing hyaline bacilliform spores (van Vloten and Gremmen, 1953). Sinclair and Lyon (2005) describe and illustrate the mature apothecia as yellowish-brown, while the early forms are dark.

Crumenulopsis pinicola (Fr.) JW Groves differs in having shorter, thick-stalked asci, 65-90(-100) X 10-13(-14) Um, and longer, fusiform ascospores, 18-30 (-35) X 3.0-4.0 Um (Groves, 1969). This is a saprobic species found on dead wood (Gremmen, 1968).

Gremmeniella abietina produces falcate multicellular conidia in a mucilaginous matrix from pycnidia on infected pines (Sinclair and Lyon, 2005). The dark brown apothecia exhibit the differences described above for C. abietina (under Taxonomy). Ascospores are ellipsoid, 4-celled, 15.2-16.1 X 3.8-4.7 Um (van Vloten and Gremmen, 1953).

DETECTION AND INSPECTION METHODS

Before cankers are large enough to cause shedding of bark, they can be detected by the production of resin that accompanies them, from the first few droplets (Gremmen, 1968) to copious flows (Butin, 1995). If mature, the dark brown to black apothecia in and around the canker must be examined microscopically to differentiate them from those of related species. If the unique spores of the Digitosporium anamorph (Sutton, 1980) can be found in pycnidia in the bark, this will be conclusive. Pycnidia also can be obtained in culture on 2.5% malt agar (Batko and Pawsey, 1964).

NOTES ON PLANTS AFFECTED

C. sororia has been reported as a pathogen on native and introduced species in various countries (Spaulding, 1961; Manap and Hayes, 1971; Hayes et al., 1981) although incidence and distribution data may not be completely accurate due to confusion with C. pinicola (Hayes and Manap, 1975).

SYMPTOMS - DESCRIPTION

Cankers begin with loosening and splitting of the bark and production of resin, which increases gradually from droplets to streams (Hayes, 1973; Butin, 1995). Internally, there is necrosis of the cambium, with (Gremmen, 1959; Manap and Hayes, 1971) or without (Hayes, 1973) dark blue to black staining of wood and bark, depending upon the tree species. On Pinus contorta, cankers occurred at nodes and in branch axils, as well as between nodes on branches (Manap and Hayes, 1971). Depending on the vigor of the tree, ridges of callus tissue may be produced annually around the canker (Butin, 1995). Stems and branches are flattened in the area of the canker and may be girdled by multiple cankers, so that trees are stunted or killed (Batko and Pawsey, 1964; Manap and Hayes, 1971; Hayes, 1973).

BIOLOGY AND ECOLOGY

Fructification (production of apothecia on infected parts) results from random outcrossing between strains (Ennos and Swales, 1987). Apothecia appear in the spring and early summer after infection (Hayes, 1980). Pycnidia are also produced in and around the canker (Batko and Pawsey, 1964). In Scotland, ascospores are released in spring to early fall months (May to September) in response to certain weather conditions (Hayes, 1975, 1980). Ascospores can remain airborne, particularly within the tree canopy, until removed by wind or rain (Hayes, 1980).

Morelet et al. (1987) report that leaf scars, particularly on older shoots, are an important infection court on Pinus halepensis. Gremmen (1968) cited bark injuries as points of infection, with frost contributing to their incidence, but it is not clear whether injury is required for infection (Hayes, 1973). Manap and Hayes (1971) list nodes, internodes and branch axils as sites for cankers on Pinus contorta.

PHYSIOLOGY AND PHENOLOGY

Within the species in a substantial geographic area of Scotland, there is a broad range of sensitivity to inhibitory monoterpenes produced by trees (Ennos & Swales, 1988) and of other fungal characteristics (Ennos and McConnell, 2003) but there is no evidence for adaptation of populations to local conditions (Ennos and Swales, 1991; Ennos and McConnell, 1995).

ENVIRONMENTAL REQUIREMENTS

In Scotland, Hayes (1977) found that incidence of infection on the introduced plantation species, Pinus contorta, was greatest in climatic zones with less rainfall and longer growing seasons. New cankers were more common on the northern and western sides of stems in those drier and warmer areas, while in areas of highest rainfall and shortest growing season, the lowest numbers occurred on the north sides and highest numbers on the western sides. Less infection was observed for southwestern and southeastern aspects. On older trees, conditions needed for infection appeared to be restricted to the lower parts of the stem. Further work on a model (Hayes et al., 1981) confirmed that incidence (% of trees with infection) was related to site elevation, aspect and exposure, but these factors could not explain variation in severity of disease.

Infection of Pinus contorta was also strongly correlated with the level of soil moisture (Craig and Hayes, 1981). Vuorinen (2000) studied the increase in number of cankers in luxuriant growth of a plantation of P. sylvestris in Finland and attributed it to the high humidity in the canopy. According to Morelet et al. (1987), cankers on P. halepensis in France increase in frequency when rainfall is above normal.

MOVEMENT AND DISPERSAL

Airborne ascospores are apparently the means of local dispersal (Hayes, 1985, 1980). Long distance movement, as with other canker-causing pathogens (Allen and Humble, 2002), could occur through transportation of bark-bearing logs, branches or wood.

ECONOMIC IMPACT

In Scotland, from 33 to 88% of the trees in stands of P. contorta were attacked (Gremmen, 1968), and increment losses of 7-40% were reported by Hayes (1973). Vuorinen (2000) reports on a plantation of Scots pine in which incidence increased from 48% to 72% despite thinning. Even if a tree is not killed, the infection can make the wood unusable (Manap and Hayes, 1971).

MANAGEMENT

Cultural control and sanitary measures: More vigorous trees are more resistant (Batko and Pawsey, 1964). Disease occurs more frequently, but not exclusively, in plantations affected by poor soil structure, inadequate drainage, and low fertility, or by damage due to exposure. Such sites should be avoided or conditions ameliorated before and after planting. Butin (1995) recommends removal of infected trees as a means of control, but the report of an increase of infection after thinning (Vuorinen, 2000) indicates that success is unlikely, at least in plantations.

Host resistance: Different provenances of Pinus species differ in susceptibility (Hayes, 1977; Stephan & Butin, 1980; Butin, 1995). A provenance should be selected for planting that is adapted to the local climate. Gremmen (1968) indicates that bark injury due to frost may increase infection: a provenance adapted to frost would be less susceptible to the fungus.

GAPS IN KNOWLEDGE/RESEARCH NEEDS:

Whether C. sororia is present in North America is in dispute. No DNA sequences are available in the GenBank database for comparison with those of any specimens. In the case of a new introduction, its likely effect, in competition with other fungi, on native species is unknown. The role of the conidial anamorph in the life cycle or epidemiology is unexplored.

References

Nomenclature

Specimens in BPI

Additional distribution data

Suggested citation: Chalkley, D. Systematic Mycology and Microbiology Laboratory, ARS, USDA. . Invasive Fungi. Crumenulopsis pine dieback -Crumenulopsis sororia . Retrieved November 21, 2009, from http://nt.ars-grin.gov/sbmlweb/fungi/index.cfm .