Crumenulopsis sororia

Pictures

Picture	Title	Caption	Copyright
Title Apothecia Caption Apothecia and apothecial initials in bark of Pinus contorta var. murrayana. Original x15. Copyright USDA-ARS/Systematic Mycology & Microbiology Laboratory	Apothecia	Apothecia and apothecial initials in bark of Pinus contorta var. murrayana. Original x15.	USDA-ARS/Systematic Mycology & Microbiology Laboratory
Title Apothecium on bark Caption Apothecium on bark of Pinus contorta var. murrayana. Original x33. Copyright USDA-ARS/Systematic Mycology & Microbiology Laboratory	Apothecium on bark	Apothecium on bark of Pinus contorta var. murrayana. Original x33.	USDA-ARS/Systematic Mycology & Microbiology Laboratory
Title Cross section of apothecium Caption Cross section of apothecium, showing marginal 'hairs'. Original x100. Note scale bar. Copyright USDA-ARS/Systematic Mycology & Microbiology Laboratory	Cross section of apothecium	Cross section of apothecium, showing marginal 'hairs'. Original x100. Note scale bar.	USDA-ARS/Systematic Mycology & Microbiology Laboratory
Title Ascus Caption Ascus. Original x400. Copyright USDA-ARS/Systematic Mycology & Microbiology Laboratory	Ascus	Ascus. Original x400.	USDA-ARS/Systematic Mycology & Microbiology Laboratory
Title Ascospores Caption Ascospores. Original x1000. Copyright USDA-ARS/Systematic Mycology & Microbiology Laboratory	Ascospores	Ascospores. Original x1000.	USDA-ARS/Systematic Mycology & Microbiology Laboratory
Title Hymenium Caption Hymenium. Original x400. Note scale bar. Copyright USDA-ARS/Systematic Mycology & Microbiology Laboratory	Hymenium	Hymenium. Original x400. Note scale bar.	USDA-ARS/Systematic Mycology & Microbiology Laboratory

Identity

Preferred Scientific Name

• Crumenulopsis sororia (P. Karst) J.W. Groves 1969

Other Scientific Names

• Crumenula sororia P. Karst 1871
• Digitosporium piniphilum Gremmen 1953

Summary of Invasiveness

C. sororia is an apothecia-forming ascomycete (cup fungus) 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 native and introduced species of Pinus. Once introduced, its small size, resemblance to related canker-causing species, and spread by airborne spores, would make control difficult.

Taxonomic Tree

• Domain: Eukaryota
•     Kingdom: Fungi
•         Phylum: Ascomycota
•             Subphylum: Pezizomycotina
•                 Class: Leotiomycetes
•                     Subclass: Leotiomycetidae
•                         Order: Helotiales
•                             Family: Helotiaceae
•                                 Genus: Crumenulopsis
•                                     Species: Crumenulopsis sororia

Notes on Taxonomy and Nomenclature

Karsten (1871) described this fungus as a species of Crumenula, but transferred it to the Godronia subgenus Heteropeziza when he synonymized Crumenula with Godronia in 1885.

Nannfeldt combined the genus with Godronia and Durandia in the genus Scleroderris (Fr.) de Not. Seaver chose to follow Karsten (1885) in placing C. sororia and Crumenula pinicola in Godronia (van Vloten and Gremmen, 1953).

Gremmen found that the four species of Crumenula on Pinaceae 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 Crumenula laricina. Where they are known, the asexual states forms are also different. Gremmen recognized C. sororia and C.pinicola in Crumenula de Not., and placed C. abietina and C. laricina in Scleroderris (van Vloten and Gremmen, 1953).

Noting nomenclatural problems with the status of the genus Crumenula, Groves (1969) established the genus Crumenulopsis for C. pinicola, as type species, and C.sororia.

Description

Apothecia stalk-less, emerging from cracked bark, often in clusters, cup- to saucer-shaped, dark-brown to black, exterior rough, somewhat hairy, inrolled when dry, interior disk exposed when damp, pale, 2 mm diameter. Asci 100-120 (90-125) x 12-13 mm, eight-spored roughly in two columns (biseriate). Ascospores hyaline, elongate-fusiform, occasionally one-septate, 18-21 (-27) x 3-5 mm. Paraphyses filiform, sometimes branched, tips upto 3 mm wide (Dennis, 1978).

Groves (1969) identifies an ectal excipulum of the apothecium, of thick-walled, dark cells forming textura angularis distinct from the textura intricata of the medullary excipulum. Van Vloten and Gremmen (1953) describe the apothecium as having marginal hairs to 100 mm long, hymenium yellow-green, stipe 300-600 mm and ascospores ellipsoidal, 12.9-30.1 x 5.7 mm, one- to four-celled. Septation in ascospores appears to increase with age; Hayes (1975) reports that it occurs after spore release.

The asexual form (Digitosporium piniphilum) produces pale-brown conidia 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 greyish 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 centre, 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 15-22.5⁰C, usually faster in the dark.

Distribution

Groves (1969) considered reports of C. sororia in the USA to be erroneous and a misidentification of Atropellis species. Lack of reports of C. sororia from other countries with temperate climates may be due to the difficulty of distinguishing it from related fungi.

Distribution Table

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.

Habitat List

Hosts/Species 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 Crumenula pinicola (Hayes and Manap, 1975).

Host Plants and Other Plants Affected

Growth Stages

Symptoms

Cankers begin with loosening and splitting of the bark and production of resin, which increases gradually from droplets to streams (Hayes, 1973; Butin et al., 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 vigour of the tree, ridges of callus tissue may be produced annually around the canker (Butin et al., 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).

List of Symptoms/Signs

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 autumn (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 Pinushalepensis. 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 and 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, P. 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, whereas 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 P. 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 Pinus 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.

Climate

Means of Movement and Dispersal

Airborne ascospores are apparently the means of local dispersal (Hayes, 1975; 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.

Pathway Vectors

Plant Trade

Impact Summary

Economic Impact

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

Risk and Impact Factors

• Invasive in its native range
• Highly mobile locally
• Has high reproductive potential
• Reproduces asexually

• Host damage
• Negatively impacts forestry

• Pathogenic

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

Detection and Inspection

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 et al., 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).

Similarities to Other Species/Conditions

Crumenulopsis pinicola differs in having shorter, thick-stalked asci, 65-90(-100) x 10-13(-14) mm, and longer, fusiform ascospores, 18-30 (-35) x 3.0-4.0 mm (Groves, 1969). This saprobic species occurs on dead wood (Gremmen, 1968).

Cenangium ferruginosum 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 mm. 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, whereas the early forms are dark.

In the related genus, Cenangium, with species on pine as saprobes or weak parasites, the ascospores are ellipsoid. In Gremmeniella, the ascospores are multi-septate.

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 for Crumenula abietina (see Taxonomy section). Ascospores are ellipsoid, four-celled, 15.2-16.1 x 3.8-4.7 mm (van Vloten and Gremmen, 1953).

Prevention and Control

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 et al. (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 and Butin, 1980; Butin et al., 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

Allen EA; Humble LM, 2002. Nonindigenous species introductions: a threat to Canada's forests and forest economy. Canadian Journal of Plant Pathology, 24(2):103-110; 37 ref.

Anon, 1964. Diseases of Widely Planted Forest Trees. US Forest Service Department of Agriculture. Washington DC, USA: United States Government Printing Office, 237 pp.

Batko S; Pawsey RG, 1964. Stem canker of Pine caused by Crumenula sororia. Transactions of the British Mycological Society, 47(2):257-61.

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

Craig M; Hayes AJ, 1981. Distribution of Crumenulopsis sororia (Karst.) Groves in relation to site and crop factors in some stands of lodgepole pine of Alberta provenance. Forestry, 54(1):75-88.

Dennis RWG, 1978. British Ascomycetes. Vaduz, Liechtenstein: J. Cramer., 585 pp.

Ennos RA; McConnell KC, 1995. Using genetic markers to investigate natural selection in fungal populations. Canadian Journal of Botany, 73:S302-S310.

Ennos RA; McConnell KC, 2003. Variation in host resistance and pathogen selective value in the interaction between Pinus sylvestris and the fungus Crumenulopsis sororia. Heredity, 91(3):193-201.

Ennos RA; Swales KW, 1987. Estimation of the mating system in a fungal pathogen Crumenulopsis sororia (Karst.) Groves using isozyme markers. Heredity, 59(3):423-430.

Ennos RA; Swales KW, 1988. Genetic variation in tolerance of host monoterpenes in a population of the ascomycete canker pathogen Crumenulopsis sororia. Plant Pathology, 37(3):407-416.

Ennos RA; Swales KW, 1991. Genetic variability and population structure in the canker pathogen Crumenulopsis sororia. Mycological Research, 95(5):521-525.

Gremmen J, 1959. A contribution to the mycoflora of pine forests in the Netherlands. Nova Hedwigia, 1:251-288.

Gremmen J, 1968. [English title not available]. (Stamkasnkers van groveden en Corsicaanse den veroorzaakt door Crumenula sororia Karst.) Nederlands Bosbouw Tijdschrift, 40:176-182.

Groves JW, 1969. Crumenulopsis, a new name to replace Crumenula Rehm. Canadian Journal of Botany, 47(1):47-51.

Hayes AJ, 1973. The occurrence of Crumenula sororia Karst. on Lodgepole Pine in the United Kingdom. Forestry, 46(2):125-138 + 3 pl.

Hayes AJ, 1975. Some preliminary observations on the distribution of Crumenula sororia spores in the atmosphere. Transactions of the British Mycological Society, 64(3):546-550 + pl.

Hayes AJ, 1977. Incidence and importance of Crumenula [Cremenulopsis] sororia on lodgepole pine. Distribution of infection in individual trees. European Journal of Forest Pathology, 7(2):105-119.

Hayes AJ, 1980. Spore liberation in Crumenulopsis sororia. Transactions of the British Mycological Society, 74(1):27-40.

Hayes AJ; Manap Ahmad A, 1975. Cultural characteristics of Crumenula sororia. Transactions of the British Mycological Society, 65(3):403-412.

Hayes AJ; Newton NG; Jolly GM; Wood J; Anderson MH, 1981. The prediction of Crumenulopsis sororia (Karst.) Groves. Incidence on lodgepole pine (Pinus contorta Dougl.) using multiple regression techniques. European Journal of Forest Pathology, 11(7):396-411.

Hayes J; Newton NG; Jolly GM; Wood J; Anderson MH, 1981. The prediction of Crumenulopsis sororia (Karst.) Groves. Incidence on lodgepole pine (Pinus contorta Dougl.) using multiple regression techniques. European Journal of Forest Pathology, 11:396-411.

Manap ABA; Hayes AJ, 1971. Crumenula sororia Karst. associated with cankering and dieback of Corsican Pine. Scottish Forestry, 25(3):185-200.

Morelet M; Thibault J; Renoux JL, 1987. Canker disease of Aleppo pine. II. Research into means of intervention. Foret Mediterraneenne, 9:119-126.

Roll-Hansen F, 1978. Fungi dangerous to Pinus contorta with special reference to pathogens from north Europe. European Journal of Forest Pathology, 8(1):1-14.

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

Smith IM; Dunez J; Lelliott RA; Phillips DH; Archer SA(Editors), 1988. European handbook of plant diseases. Oxford, UK: Blackwell Scientific Publications.

Spaulding P, 1961. Foreign diseases of forest trees of the world. An annotated list. Agriculture Handbook No. 197. Washington, D. C., USA: U. S. Department of Agriculture. pp. 361.

Stephan BR; Butin H, 1980. [English title not available]. (Krebsartige Erkrankungen an Pinus contorta- Herkünften.) European Journal of Forest Pathology, 10:410-419.

Sutton BC, 1980. The Coelomycetes. Fungi imperfecti with pycnidia, acervuli and stromata. Wallingford, UK: CAB International.

Vloten HVan; Gremmen J, 1953. Studies on the Discomycete genera Crumenula de Not. and Cenangium Fr. Acta Botanica Neerlandica, 2(2):226-41.

Vuorinen M, 2000. Canker disease of Scots pine caused by Crumenulopsis sororia. Metsanduslikud Uurimused [Tree diseases in the first generation stands and other Nordic forest pathology problems. Proceedings of the Nordic/Baltic meeting on forest pathology, Sagadi, Estonia, 17-22 June 2000.], 34:61-63.

Contributors

10/09/09 Original text by:

Distribution Maps