Preferred name: Gremmeniella abietina
Authority: (Lagerberg) Morelet
Taxonomic position: Fungi: Ascomycota: Pezizomycotina: Leotiomycetes: Helotiales: Helotiaceae
Other scientific names: Ascocalyx abietina (Lagerberg) Schläpfer-Bernhard, Brunchorstia destruens Eriksson, Brunchorstia pinea var. cembrae Morelet, Brunchorstia pinea var. pini Morelet, Brunchorstia pinea (Karsten) von Höhnel, Brunchorstia pini Allescher, Crumenula abietina Lagerberg, Crumenula pinea (Karsten) Ferdinandsen & C.A.Jørgensen, Excipulina pinea Karsten, Godronia abietina (Ellis & Everhart) Seaver, Lagerbergia abietina (Lagerberg) J.Reid, Scleroderris abietina (Lagerberg) Gremmen, Scleroderris lagerbergii Gremmen, Septoria pinea Karsten
Common names in English: brunchorstia disease of pine, canker of conifers, dieback of pine, scleroderris canker of conifers (US), shoot blight of pine
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Notes on taxonomy and nomenclature EU Categorization: PZ Quarantine pest (Annex III)
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EPPO Code: GREMAB

The host range of G. abietina is mostly confined to Pinus species and other conifers such as Abies spp., Picea spp., Larix spp., and Pseudotsuga spp., of which two major European host species (Pinus sylvestris and Picea abies) occur widely in the EPPO region. Abies sachalinensis and P. contorta are also considered important hosts (Jeger et al., 2017). The North American race occurs in the USA and Canada mainly on Pinus resinosa, Pinus banksiana, and Pinus contorta, where it causes damage on low parts of trees that remain under snow cover during the winter (Petrini et al., 1989). The European race generally infects the entire crown of hosts, and it is found on several different hosts belonging mainly to Pinus spp. in Europe and North America. The Asian race has been found only in Japan on A. sachalinensis (Jeger et al., 2017). The two- and three-needled pines are most susceptible; five-needled pines and spruces are much less susceptible or tolerant while other conifers seem to be resistant (Sinclair & Lyon, 2005). For additional information, see Sinclair & Lyon (2005).

Host list: Abies balsamea, Abies nordmanniana subsp. equitrojani, Abies sachalinensis, Larix lyallii, Picea abies, Picea glauca, Picea jezoensis, Picea mariana, Picea omorika, Picea rubens, Picea sitchensis, Pinus banksiana, Pinus cembra, Pinus contorta, Pinus densiflora, Pinus halepensis, Pinus koraiensis, Pinus monticola, Pinus mugo, Pinus nigra subsp. laricio, Pinus nigra subsp. pallasiana, Pinus nigra, Pinus pinaster, Pinus pinea, Pinus ponderosa, Pinus radiata, Pinus resinosa, Pinus rigida, Pinus sabiniana, Pinus strobus, Pinus sylvestris, Pinus wallichiana, Pseudotsuga menziesii

G. abietina is a destructive pathogen of conifers in North, Central, and South Europe, north-eastern North America, and East Asia (Botella & Hantula, 2018). G. abietina causes a disease known as Scleroderris canker in North America and Brunchorstia dieback in Europe (Yokota et al., 1974; Skilling et al., 1984; Petrini et al. 1989; Hudler & Neal, 1990; Sinclair & Lyon, 2005, Thompsen, 2009; Botella & Hantula, 2018).

EPPO Region: Austria, Belarus, Belgium, Bulgaria, Czech Republic, Denmark, Estonia, Finland, France (mainland), Georgia, Germany, Greece (mainland), Italy (mainland), Lithuania, Montenegro, Netherlands, Norway, Poland, Romania, Russia (Central Russia, Eastern Siberia, Far East, Northern Russia), Serbia, Slovakia, Slovenia, Spain (mainland), Sweden, Switzerland, Türkiye, United Kingdom (England, Scotland)
Asia: Japan (Hokkaido), Korea, Republic
North America: Canada (Alberta, British Columbia, Manitoba, New Brunswick, Newfoundland, Nova Scotia, Ontario, Québec), United States of America (Maine, Michigan, Minnesota, New Hampshire, New York, Wisconsin)

The ascomycete fungus G. abietina is a pathogen which causes cankers on stems and trunks, dieback and death of the trees. The germinating conidia or ascospores enter the apical buds and developing shoots, especially during cool, wet springs (Venier et al., 1998; Witzell & Karlman, 2000; Thompsen, 2009). The initial attack of G. abietina typically starts in the lower part of the crown and spreads to branches in the upper part of the crown, and then towards the stem, causing perennial cankers (Hellgren & Barklund, 1992; Sinclair & Lyon, 2005). Wounded needles, buds and shoots are particularly susceptible to infection. Conidia and ascospores are both infectious, however ascospores are relatively less important in disease spread (Sinclair & Lyon, 2005). In Europe, conidia and ascospores are released during of periods of wet weather, conidia are dispersed mainly in water, ascospores in air. Pycnidia starts to release conidia in late spring, whereas apothecia begin to release ascospores in summer (Hellgren & Barklund, 1992; Sinclair & Lyon, 2005). Infection occurs primarily in spring and summer, but it may be as late as October (Sinclair & Lyon, 2005). Needle bases turn orange to brown while the tip may be still green, and ultimately fall off (Hellgren & Barklund, 1992; Sinclair & Lyon, 2005). Colonization proceeds both inter- and intracellularly facilitated by hyphal secretion of different enzymes; shoots start dying, in the spring following infection, from the tips (Gremmen, 1972; Sinclair & Lyon, 2005). Small, black pycnidia develop during the first and second years of symptomatic infection and appear at the base of dead needles or on dead shoot tips throughout the year; but more commonly in the spring and early autumn (Gremmen, 1972; Sinclair & Lyon, 2005). Pycnidia release conidia, completing the disease cycle (Sinclair & Lyon, 2005). The fungus overwinters as mycelium or as immature fruiting bodies in the conifer host. G. abietina is seasonal in its development in the host plant and sexual reproduction and completion of the whole pathogen cycle takes two years; apothecia occur more commonly in the same place where pycnidia were located one year after the shoots die (Gremmen, 1972; Hellgren and Barklund, 1992; Sinclair & Lyon, 2005). In addition, the ambient temperature at this time influences both the number of ascospores that are discharged per apothecium and how soon dispersal commences. Maximum spore discharge takes place at approximately 17°C. If free water is available in the form of rain for 4–8 h at this temperature, major spore release will take place (Skilling, 1972). Snowy winters also frequently promote damage by G. abietina (Witzell and Karlman, 2000). This results in significant loss of foliage, further weakening of the trees due to secondary attack by other fungi and insects, and finally death. G. abietina can grow at temperatures of -6°C. This facilitates tree colonization due to the suppression of the immune system of trees during the winter, and disease appears frequently in sites which are very wet for a long time (such as frost pockets and cold air drainages) and where snow lingers in spring (Sinclair & Lyon, 2005).

Symptoms

Generally, G. abietina initially infects and kills buds and the current-year shoots. The pathogen can then remain latent for several years or continue to grow along the branch towards the main stem (Skilling et al., 1986; Bernhold, 2008). The North American and European races cause similar symptoms on susceptible hosts with abundant canker formation and production of both pycnidia and apothecia on smaller trees, particularly on those covered with snow in the winter (Uotila, 1985; Barklund, 1990; Hamelin et al., 1996; Bernhold, 2008). Initial infection by G. abietina occurs in developing shoots in the spring and resinous lesions form primarily during the host’s period of dormancy in cortical tissue of the first- or second-year twigs, then they extend into needle bases and buds (Gremmen, 1972; Sinclair & Lyon, 2005). However, the first symptoms may not appear until the following winter when resin exudation can be observed on the buds (Gremmen, 1972). Typically, needle bases turn orange-brown by early spring and the discoloration gradually extending to the needle tips and symptomatic needle clusters can be pulled from twigs readily and needles can drop during late spring and summer (Sinclair & Lyon, 2005). The necrosis formed under the short shoots weakens the stability of the needles (they easily fall out) and cuts off all the transport of water and nutrients into the needles (Roll-Hansen, 1964; Skilling, 1972). The characteristic yellow colouration of the xylem tissues and distorted shoots can also be seen (Read, 1967; Skilling, 1972). Consequently, the previous year’s needles are often bent down and red to brown, starting from the base and moving towards the tip (Roll-Hansen, 1964; EPPO, 2009). Buds on twigs with discoloured needles frequently do not open and resin droplets appear on the bark of the current year’s shoots (Sinclair & Lyon, 2005; EPPO, 2009). After about one year, the dead shoots loose most or all of their red-brown needles and appear dry (Bernhold, 2008). One year later bunches of light-green needles may develop from adventitious buds, present at the base of the dead shoots and sometimes giving the appearance of small witches' brooms (Roll-Hansen, 1964; Skilling, 1972; EPPO, 2009). G. abietina mycelia can survive up to eight years in P. sylvestris in symptomless shoots (Hellgren & Barklund, 1992). G. abietina can remain in the shoots during unfavourable conditions and rapidly recolonize a stand when conditions become favourable for the pathogen (Bernhold, 2008).

G. abietina can causes larger necroses in the inner tissue of stems and branches resulting in cankers on stems and branches (Skilling, 1972). The cambial region in necrotic lesions caused by the North American race is often become discoloured or turns yellow-green due to a pigment produced by the pathogen (Sinclair & Lyon, 2005). Moreover, trunk cankers caused by the North American race are elongate, resinous, and usually have a greenish discoloration while the European race causes death of apical buds and adjacent needled on P. banksiana and P. contorta (tip blight) and stem cankers are quite rare (Sinclair & Lyon, 2005). Stem cankers caused by the biotype LTT of G. abietina are rare in Sweden, even though small cankers on branches do occur (Hellgren & Högberg, 1996; Bernhold, 2008). On the other hand, cankers on the main stem caused by the biotype STT of G. abietina are frequently found in Northern Sweden, especially on P. contorta, and these are formed after infection through the base of diseased branches and through bark damage caused by snow, frost, and ice formation (Bernhold, 2008).

Morphology

Pycnidia of G. abietina develop on needles and stems after appearance of symptoms on needles (Sinclair & Lyon, 2005). In this species, they are generally more common than apothecia (EPPO, 2009). Pycnidia form singly or in clusters in the bark of dead twigs or needle bases; they are irregular in shape, multilocular with one or more fertile cavity, dark-brown to black on the surface and white within, stromatic, up to 1 mm wide (Roll-Hansen, 1964; Skilling, 1972; Sinclair & Lyon, 2005; EPPO, 2009). Pycnidia produce conidia in a mucilaginous matrix. Conidiophores completely line the inside of the pycnidial cavity, they are hyaline, cylindrical. Conidia are individually colourless, usually four celled, sometimes five-seven celled, hyaline, cylindrical, somewhat curved, 25–40 × 3.0–3.5 µm and have pointed ends (Sutton, 1980; Sinclair & Lyon, 2005). Microconidia are 5 x 3 µm; they have been also found in pycnidia of G. abietina on many Pinus species in Europe and North America (Roll-Hansen, 1964; Skilling, 1972; Sutton, 1980) and their function is still unclear (Bergdahl, 1984; Sinclair & Lyon, 2005).

Brown cuplike apothecia appear in the spring on needles and twigs which died 1–2 years ago (Gremmen, 1972; Bergdahl, 1984; Sinclair & Lyon, 2005). Apothecia are gregarious, erumpent, superficial, about 1 mm in diameter, slightly taller than wide, measure 400–1200 × 120–250 μm with short stalks and the fertile inner surface is cream-coloured (Sutton, 1980; Sinclair & Lyon, 2005). Asci subclavate, short-stipitate, inoperculate, eight-spored, 100–120 x 6.5–10.5 µm and ascus wall bitunicate. Ascospores are colourless, biseriate, 3-septate, typically 4-guttulate with rounded ends, hyaline, sometimes slightly curved, 15–22 x 3–5 µm (Punithalingam & Gibson, 1973; Sutton, 1980; Sinclair & Lyon, 2005).

Detection and inspection methods

G. abietina can be identified based on the species’ morphological structures following the EPPO diagnostic protocol PM 7/92 (1): Gremmeniella abietina. If mature fruiting structures are present, G. abietina can easily be identified in vivo. In the absence of visible fruiting structures, the symptomatic samples should be incubated in a moist chamber or used for culturing to induce sporulation and then identification is possible using the classical morphological examination; the presence of pycnidia and the conidia as well as the ascomata and ascospores can distinguish G. abietina. Culture media and isolation techniques from needles and shoots are also described in the EPPO diagnostic protocol (EPPO, 2009, 2019).

Pine seedlings in nurseries should be inspected for orange to brown discoloration at the bases of needles in early May. By July, needles and branch tips of infested plants become brown. Needles may fall down from branch tips when the slightest pressure is applied. In young pine trees, green discoloration appears beneath the bark of dead branches. Stem cankers are rare but small branch cankers are commonly found. Throughout the year, but in particular in the spring and the early autumn, black pycnidia or light-brown apothecia are likely to be visible at the base of dead needles or on dead branch tips.

In forests, the earliest visible symptoms of the disease are indicators of the presence of infection in the buds or shoots. The most obvious early symptom is the orange to brown discoloration of the needle bases in the spring prior to shoot elongation.

The three races (Asian, European, and North American) within G. abietina have been distinguished by immunological and other methods (Dorworth & Krywienczyk, 1975). Since the European and North American races do not differ morphologically from each other, several molecular approaches have been used to allow their identification (Hogberg, 1995; Hamelin et al., 1996, 2000; Hantula & Muller, 1997; Zeng et al., 2005). Then, three biotypes have been distinguished within the European race based on disease symptoms and conidia morphology (Hamelin et al., 1993; Zeng et al., 2005; Botella et al., 2015; Lamarche et al., 2015). Different varieties, races, and biotypes of G. abietina can be also identified and separated using different DNA methods (Hamelin et al., 1996, 1998, 2000; Hantula & Muller, 1997; Zeng et al., 2005; Botella et al., 2015; Lamarche et al., 2015) and some other methods (Appendix 1 of the EPPO diagnostic protocol: EPPO, 2009, 2019), but such differentiation is not required for quarantine purposes; given the uncertainty about the taxonomic position of the varieties within G. abietina, none of these tests are recommended (EPPO, 2009).

The presence of G. abietina on shoots, needles and roots can be revealed using G. abietina specific primers for conventional PCR (developed by Dr. Elna Stenström, Swedish University of Agricultural Sciences, Sweden) (Adomas & Asiegbu, 2006).

G. abietina can survive in an endophytic stage for an uncertain period of time during unfavourable conditions for the pathogen in symptomless shoots (Petrini et al., 1989; Hellgren & Barklund, 1992). Therefore, it might be moved over long distances in infected asymptomatic plants (Jeger et al., 2017). Under favourable wet conditions, conidia released from the infected tissues are dispersed by a water splash mechanism (Thomsen, 2009). Long-distance dispersal of the fungus is considered to occur largely through wind-borne ascospores (Sinclair & Lyon, 2005). The widespread distribution of the pathogen may lead to infection from conidia or ascospores entering the nursery site of production from surrounding areas (Jeger et al., 2017). Transport of infected nursery stock or movement of infected Christmas trees may provide alternative means of long-distance dispersal (Patton et al., 1984; Santamaría et al., 2007; Jeger et al., 2017).

Economic impact

Scleroderris canker caused by G. abietina is a major disease of pines in snowy regions of Europe and eastern North America (Sinclair & Lyon, 2005; Bernhold, 2008). It kills seedlings, saplings, and stunts and deforms survivors, and reduces timber quality due to the trunk cankers (Sinclair & Lyon, 2005). The European race of G. abietina is more aggressive than the North American race, in which can be seen on most of their common hosts, and the European race kills shoots and causes cankers and dieback on trees of all sizes (Sinclair & Lyon, 2005). Large scale outbreaks may occur in years with long period of cool and moist weather in the spring. Tree mortality depends on the size of the host at the time of infection: nursery seedlings and saplings are much more susceptible and die soon after infection, usually during the first year, whereas larger trees gradually die over several years. Large stem cankers reduce height growth (Bernhold, 2008) and may eventually kill the tree by strangulation (Roll-Hansen, 1964). In Fennoscandia, G. abietina is the most severe shoot pathogen of native P. sylvestris (Roll-Hansen, 1964; Wulff et al., 2006) and introduced P. contorta and P. cembra; it also damages P. abies (Bernhold, 2008). So far, the most severe outbreak of G. abietina in Sweden took place in 2001–2003 and almost 500 000 ha of middle-aged pine-dominated forests were attacked. To control the disease, many P. sylvestris stands were thinned or clear-cut, resulting in large loses for the forest owners due to the costs of the phytosanitary management and reduction in income (Wulff et al., 2006). G. abietina also destroyed many plantations of P. resinosa in Newfoundland, Southern Quebec, Canada, and adjacent regions of the USA (Sinclair & Lyon, 2005)

G. abietina is most damaging to the stands of conifers growing close to the limit of their species’ ranges and its attacks are favoured by shaded conditions, by dense, badly aerated plantations in which humidity is high, and by weather damage, such as temperature oscillations during shoot elongation.

Control

Complete eradication of the pest is difficult due to the latent nature of the disease (Santamaría et al., 2007). However, suitable control measures could reduce its spread and virulence. In the field, silvicultural measures have been recommended for the control of G. abietina such as maintaining a suitable stand density, planting resistant species (Sinclair & Lyon, 2005), or removal of diseased trees from the stand (Aalto-Kallonen and Kurkela, 1985). Moreover, during reforestation, planting of tolerant and resistance hosts is recommended (Santamaría et al., 2007). Also, as pathogen’s attacks are facilitated by shaded conditions, by dense, badly aerated plantations, appropriate spacing between plants and thinning may reduce the risk of infection, and pruning of the lower branches has proved to be a very effective method of reducing the incidence of G. abietina on early stage of outbreak when only a small number of trees are infested (Laflamme, 1999). The damage to new plantation on sites conducive to infection can be minimized by planting resistant tree species (Witzell & Karlman, 2000). Delaying pine planting until after two growing seasons following the harvesting of diseased pine trees is recommended (Laflamme and Rioux, 2015) and slash burning or complete removal of the infected slash is needed to minimize the infection risk (Bernhold et al., 2006).However, once G. abietina is established in a plantation, it is almost impossible to control it.

Chemical control in the field is possible but expensive. It also might have deleterious impact on biodiversity (including non-target fungi) and can increase pathogen resistance to the fungicide. In general, careful selection of disease-free planting material and suitable planting sites (e.g. the sites not characterized by cool and wet springs and/or by risk of frost damage) at some distance from infested plantations are important control measures. However, in nurseries the disease may be controlled by using fungicides. Several fungicides have traditionally been recommended against this pathogen, such as, chlorothalonil, propiconazole and azoxystrobin applied from May to mid-August were reported as the most effective fungicide against both North American and European races of G. abietina, if spraying was carried out in the spring when temperatures were above 0°C (Santamaría et al., 2007; Romeralo et al., 2015). Although use of fungicides against fungal pathogens might be a useful control strategy in the short term, there is currently an increasing interest in finding effective biological control methods, and recent EU legislation (Council Directive, 2009) recommended sustainable forest management and protection of forests and their biodiversity giving priority to non-chemical methods. Identifying alternatives to chemicals (e.g., use the biological control agents or fungal endophyte filtrates) is currently a priority and has been widely studied (Laflamme 1999; Santamaría et al., 2007). Some of these alternative methods have shown a strong antagonistic activity against G. abietina (Romeralo et al., 2015).

Phytosanitary risk

G. abietina has not been classified as a quarantine pest by EPPO, but the species is a quarantine pest in three EPPO countries (Morocco, Tunisia and Israel) (EPPO, 2023). In Europe, G. abietina has generally been regarded as widespread and it has likely reached the limits of its natural distribution. According to the Implementing Regulation (EU) 2020/2210, G. abietina is a regulated pest of Abies, Larix, Picea, Pinus, and Pseudotsuga, intended for planting, other than seeds, for Protected Zones in Annex III (List of protected zones and the respective protected zone quarantine pests and their respective codes) for Ireland (EU, 2020).

Planting material of host tree species of G. abietina should be chemically treated with the fungicide chlorothalonil prior to movement. Before export to countries free from the pathogen, Christmas trees should be inspected for cankers during the summer before trading. Immersion of diseased seedlings in warm water (55°C) and immersion or spraying with dilute sodium hypochlorite eradicated the pathogen with no apparent loss in needle colour or retention (Hudler and Neal, 1990). Regulatory action by the USA and Canada now prohibits the movement of Christmas trees and nursery stock from areas where the European strain is present.

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CABI and EFSA resources used when preparing this datasheet

CABI Datasheet on Gremmeniella abietina: https://www.cabidigitallibrary.org/doi/10.1079/cabicompendium.25892

EFSA Panel on Plant Health (PLH), Jeger, M, Bragard, C, Caffier, D, Candresse, T, Chatzivassiliou, E, Dehnen-Schmutz, K, Gilioli, G, Gregoire, J-C, Jaques Miret, JA, MacLeod, A, Navajas Navarro, M, Niere, B, Parnell, S, Potting, R, Rafoss, T, Rossi, V, Urek, G, Van Bruggen, A, Van der Werf, W, West, J, Winter, S, Boberg, J, Gonthier, P and Pautasso, M (2017) Scientific Opinion on the pest categorisation of Gremmeniella abietina. EFSA Journal 15(11), 5030, 30 pp. https://doi.org/10.2903/j.efsa.2017.5030

This datasheet was extensively revised in 2023 by Kateryna Davydenko, the Ukrainian Research Institute of Forestry and Forest Melioration and the Swedish University of Agricultural Science. Her valuable contribution is gratefully acknowledged.

EPPO (2024) Gremmeniella abietina. EPPO datasheets on pests recommended for regulation. https://gd.eppo.int (accessed 2024-11-07)

This datasheet was first published in  'Quarantine Pests for Europe' in 1992 and revised in 1997, as well as in 2023. It is now maintained in an electronic format in the EPPO Global Database. The sections on 'Identity', ‘Hosts’, and 'Geographical distribution' are automatically updated from the database. For other sections, the date of last revision is indicated on the right.

CABI/EPPO (1992/1997) Quarantine Pests for Europe (1^st and 2^nd edition). CABI, Wallingford (GB).