Preferred name: Atropellis piniphila
Authority: (Weir) Lohmann & Cash
Taxonomic position: Fungi: Ascomycota: Pezizomycotina: Leotiomycetes: Helotiales: Godroniaceae
Other scientific names: Atropellis arizonica Lohman & Cash, Cenangium piniphilum Weir
Common names in English: branch canker of pine, trunk canker of pine, twig blight of pine
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Notes on taxonomy and nomenclature EPPO Categorization: A1 list
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EPPO Code: ATRPPP

Pinus contorta (lodgepole pine) is the major host, but A. piniphila can also attack P. albicaulis (whitebark pine), P. banksiana (jack pine), P. densiflora (Japanese red pine), P. echinata (shortleaf pine), P. jeffreyi (Jeffrey pine), P. monticola (western white pine), P. nigra (black pine), P. ponderosa (ponderosa pine), P. taeda (lobolly pine), and P. virginiana (Virginian pine) (Sandoval et al., 1979; Sinclair & Lyon, 2005).

Host list: Pinus albicaulis, Pinus banksiana, Pinus contorta, Pinus densiflora, Pinus echinata, Pinus jeffreyi, Pinus monticola, Pinus nigra, Pinus ponderosa, Pinus taeda, Pinus virginiana

Atropellis piniphila was commonly found in North America, where it occurs from British Columbia and Saskatchewan to California and New Mexico, except central Rocky Mountain region and, occasionally in South Dakota and southeastern USA. The fungus mainly attacks branches and main stems, causing elongate cankers on stems of young trees (Sinclair and Lyon, 2005; Cerezke et al., 2014). No information was found in the literature and databases concerning the presence of A. piniphila in other continents.

North America: Canada (Alberta, British Columbia, Northwest Territories, Saskatchewan), United States of America (Alabama, Arizona, California, Idaho, Montana, New Mexico, North Carolina, Oregon, South Dakota, Tennessee, Washington)

The life cycle of A. piniphila is similar to those of all Atropellis species (Lightle, 1973). Trees can be infected by A. piniphila through ascospores. Ascospores can penetrate undamaged bark or needles of susceptible hosts and start to germinate. The fungus causes cankers and produces stromata containing conidia and apothecia in the central sunken canker zone. Conidia are released as a creamy, sticky mass (Sinclair and Lyon, 2005; Lockman 2005). Apothecia may appear up to 4 years of infection and continue to form on the canker. Ascospores are dispersed by wind, mainly in summer to early autumn. Ascospores can infect stem wounds and young branches (Sinclair and Lyon, 2005).  Infection can be asymptomatic for a long time, and apothecia with ascospores can form after a period of 2–5 years on branches and stems of infected trees (Sinclair and Lyon, 2005). Latent infection can even last for a period of up to 25 years (Hiratsuka, 1987; Lockman, 2005). Apothecia and ascospores production continue each year until a few years after death of the host on logs in heavy shaded places (Hopkins, 1969; Lockman 2005).

For further details, see also Anon. (1963), Hopkins (1963), Sinclair and Lyon (2005), EFSA (2014, 2017).

Symptoms

Infection can remain asymptomatic for a long time and the first visual signs of infection can appear in 2–5 years on small branches and stems of young, slightly and severely weakened trees, or 20 or more years in large, vigorous trees (Sinclair and Lyon, 2005). Incipient cankers show no external sign of the underlying infection. Dark-brown, necrotic spots, 5–10 mm in diameter, occur within the bark, possibly enclosed by a single layer of wound tissue. The first visual typical symptoms and signs of all Atropellis species canker are a resin droplet on the bark surface, and subsequently huge amounts of fresh resin at the margin of cankers (Lockman, 2005). Cankers generally expand each year, modifying the damaged wood which becomes resin‐soaked and blue-stained. The fungus penetrates sapwood rapidly but goes into heartwood more slowly. At canker tips a reddish‐brown stain often develops in the sapwood between the bark and the nearest invaded (blue‐black) sapwood. Bark is often cracked at the margins of cankers. Ascospores of A. piniphila are formed in ascomata that are produced in stromata on the surface of the bark over the cankers, in the central sunken canker zone (Hopkins and Callan, 1991). On P. contorta, the larger the diseased stem is, the longer the fruiting of A. piniphila takes and it may be delayed from 4–5 years on small stems to 25 years or more on large ones (Sinclair and Lyon, 2005).

Cankers caused by A. piniphila are elongated and flattened, but deep and covered with bark which is cracked; they occur on stem and young branches. Multiple stem cankers may be found quite often. Fast growing A. piniphila cankers on ponderosa pine can exceed 3 m in length and the elongation rate of cankers has been estimated at about 5 cm per year (Hopkins and Callan, 1991).

For additional information see also Boyce (1961), Anon. (1963), Hopkins (1963), Hopkins and Callan (1991), Sinclair and Lyon (2005), EFSA (2014, 2017).

Morphology

There is a characteristic blue-black staining of the wood beneath cankers. A red or brown discoloration is usually present in the xylem at the edge of the blue-black zone. 

Apothecia of A. piniphila are small, 2–4 mm in diameter, cuplike, erumpent, black on the outside, with a brown interior, irregularly disc-shaped with a short central stalk, arising initially on cankers 2 and more year old and developing annually thereafter on bark stem (Sinclair and Lyon, 2005). Ascospores hyaline, fusiform, one or two cells, 16–28 x 4.7 µm. The spores are rod shaped, very thin-walled, hyaline, aseptate, cylindrical, rounded at the ends and possess a mucilaginous coat; 4–6 x 1.0–1.5 µm (Sinclair and Lyon, 2005).

For further details see Reid and Funk (1966), Sinclair and Lyon (2005).

Detection and inspection methods

Most stem cankers start as infections on undamaged bark in the vicinity of branch whorls (Hopkins & Callan, 1991). The presence of the elongated canker is the main symptom for disease identification. Massive resin flow can be seen emerging from stem cankers, as well as dark blue or black staining in sapwood under a canker, small black cup-shaped apothecia on canker margins, the vertical seams on stem because stems seem ridged, dead flagged branches occur throughout an infected tree (Dunham 2008). Infections are most numerous on the northern sides of stems; very few cankers develop on the southern sides of stems (Hopkins & Callan, 1991). Atropellis spp. may be identified using a colorimetric test: a fragment of apothecia turns 5% aqueous KOH a bluish green colour (Atropellis pinicola, A. piniphila, and A. tingens). A. apiculata will turn the solution chocolate brown (Lochman and Cash, 1940).

Atropellis species can be differentiated from one another by the shape, size and number of cells of their hyaline ascospores. Ascospores of A. piniphila are fusiform, one or two cells, 16–28 x 4.7 µm (see section on morphology above). There is one nucleotide sequence for an A. piniphila strain (isolate CBS 197.64, registration date 20 September 2019, DOE Joint Genome Institute) in GenBank ; accessed 13 June 2022). Currently, differentiation of Atropellis species is based on the morphological and culture characteristics listed above.

Imported timber of Pinus spp. from countries where the disease occurs should have had the bark removed before inspection. However, it is possible that removal of bark may be ineffective as a safeguard if it does not eliminate superficial or deep cankers which may contain mycelium and/or apothecia, and so any material with canker lesions should be carefully inspected. Particular attention should be paid to the younger branches and twigs of growing material of Pinus consignments from countries where the disease occurs (Webster and Weber, 2007).

A. piniphila spreads with plants, wood, and isolated bark (EFSA, 2017). 

Under natural conditions, Atropellis spp. spread by ascospore dispersal within pine stands. Ascospores are formed in ascomata that are produced in stromata on the surface of the bark over the cankers, in the central canker zone (Hopkins and Callan, 1992). Under wet conditions, ascospores are forcibly ejected into the air and are disseminated, primarily by wind, over up to 100 m from the inoculum source (Allen, 1994; Lockman, 2005). Therefore, debarked wood, even though it is affected by A. piniphila, cannot transfer the pest by ascospores. In international trade, logs with the bark attached may contain ascospores or traces of mycelium, as may cankers on younger branches and twigs of growing material. Under artificial conditions when infected wood (without bark) was placed in contact with another piece of wood, mycelium could colonize a new piece of wood (Hopkins, 1963). However, there is no evidence that this could happen during transport (EFSA, 2014; Cobb and Metz, 2017). The canker caused by Atropellis spp. is not known to be transmitted by Pinus fruit or seeds. It may also spread over long distances by movement of infected host plants for planting, cut branches, wood or isolated bark (EFSA, 2014).

Economic impact

A. piniphila and A. pinicola are two species of economic importance, however A. piniphila is the most important pathogen among Atropellis spp. The fungus causes a serious resinous canker of P. contorta, particularly in trees 5–25 years old in overcrowded, pure stands. Trunk cankers on P. contorta reduce the value of trees for timber and paper pulp. On P. ponderosa, A. piniphila causes long cankers while on other pines, only a minor twig blight occurs. In addition to deformation, infected bark adheres to the underlying wood, so preventing effective debarking. Damage caused by A. piniphila is most common in young dense forests of P. contorta where the fungus can kill and deform numerous trees (Sinclair and Lyon, 2005).

Control

Cultural methods such as thinning of overcrowded stands, use of a mix of species or an alternative, non-susceptible species for reforestation purposes, removal and burning of infected trees with cankers or high level of infection (Thomas and Pickel, 2010). Buffer zone (at least 100 m) between previously infected trees and regeneration may help to prevent infection, but no chemical or biological control methods have been developed (Thomas and Pickel, 2010; EFSA, 2014).

Phytosanitary risk

A. piniphila is a North American fungal pine pathogen which has not yet been reported in the EPPO region. Its risk of entry (for the EU) was assessed by the EFSA Panel (EFSA, 2017) as close to zero under the current regulatory situation. Nevertheless, while A. piniphila may be introduced in the EU, the same or higher impacts as those observed in North America are to be expected, mainly due to the lack of knowledge on the susceptibility of some native and exotic pines such as P. contorta, P. taeda, and P. nigra which are important in the EPPO region (EFSA, 2017).

EPPO member countries are recommended to regulate A. pinicola as quarantine pest of Coniferae (EPPO A1 List) (EPPO, 2021). Importing countries may prohibit plants, wood with bark, and isolated bark of Pinus spp. from North America. For EU countries, wood or isolated bark originating in Canada and the USA, Annex II of Regulation (EU) 2016/2031 prescribes that an official statement shall certify that consignment has undergone heat treatment, or chemical pressure impregnation, or fumigation. If wood of Pinus spp. is imported from North America, the consignment must have been debarked or processed (EPPO, 2018). The introduction into the EU (and circulation within) of plants of Pinus spp., which are host plants for Atropellis spp., originating from non-European countries, is forbidden.

Allen E (2014) Review of heat treatment of wood and wood packaging. NAPPO (North American Plant Protection Organization), Raleigh, North Carolina, USA. 35 pp. 

Anonymous (1963) Atropellis canker of pine. In: Internationally dangerous forest tree diseases. Miscellaneous Publication of the Forest Service, US Department of Agriculture No. 939, pp. 84–85.

Boyce JC (1961) Forest pathology (3rd edition). McGraw Hill Book Co. Inc., New York, USA. pp. 244–255.

Cerezke HF, Dhir NK & Barnhardt LK (2014) Review of Insect and Disease Challenges to Alberta Coniferous Forests. Alberta Government, Edmonton, Canada, 126 pp. 

CMI (1981) Distribution Maps of Plant Diseases No. 543 (edition 1). CAB International, Wallingford, UK.

CMI (1981) Distribution Maps of Plant Diseases No. 544 (edition 1). CAB International, Wallingford, UK.

Cobb RC & Metz MR (2017) Tree diseases as a cause and consequence of interacting forest disturbances. Forests 8, 147. 

Dunham PA (2008) Incidence of insects, diseases, and other damaging agents in Oregon forests. USDA, Forest Service, Pacific Northwest Research Station, Portland, Oregon, USA. 100 pp. 

European Food Safety Authority (EFSA) Baker R, Gilioli G, Behring C et al. (2019) Report on the methodology applied by EFSA to provide a quantitative assessment of pest‐related criteria required to rank candidate priority pests as defined by Regulation (EU) 2016/2031. EFSA Journal 17(6), e05731, 61 pp. https://doi.org/10.2903/j.efsa.2019.5731 

EFSA Panel on Plant Health (PLH) (2017) Jeger M, Caffier D, Candresse T et al. Pest risk assessment of Atropellis spp. for the EU territory. EFSA Journal 15(7), e04877, 46 pp. https://doi.org/10.2903/j.efsa.2017.4877 

EFSA Panel on Plant Health (PLH) (2014) Scientific Opinion on the pest categorisation of Atropellis spp. EFSA Journal 12(12), 3926, 33 pp. https://doi.org/10.2903/j.efsa.2014.3926

EPPO (2018) EPPO Standard PM 8/2(3) Commodity-specific phytosanitary measures. Coniferae. EPPO Bulletin 48 (3), 463–494.

EPPO (2021) EPPO Standard PM 1/002(30). EPPO A1 and A2 lists of pests recommended for regulation as quarantine pests. https://gd.eppo.int/standards/PM1/ [last accessed 01 August 2022].

EPPO (2022) EPPO Global Database page on Atropellis piniphila https://gd.eppo.int/taxon/ATRPPP [last accessed 13 July 2022].

EPPO (1979) Data sheets on quarantine organisms No. 5, Atropellis spp. EPPO Bulletin 9(2).

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Hiratsuka Y (1987) Forest tree diseases of the prairie provinces. Canadian Forest Service Inf. Rep., 3, No. NOR-X-286. 297 pp. 

Hopkins JC (1963) Atropellis canker of lodgepole pine. Etiology, symptoms and canker growth rate. Canadian Journal of Botany 41, 1535–1545.

Hopkins JC & Callan BE (1992) Atropellis canker. Canadian Forest Service, Pacific Forestry Centre, Victoria, B.C. Forest Pest Leaflet, Vol. 25.

Lightle PC (1973) Atropellis canker of pines. US Department of Agriculture, Forest Service., Vol. 138

Lockman B (2005) Management guide for Atropellis canker. USDA Forest Service, Washington, DC, USA.

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Webster J & Weber R (2007) Introduction to Fungi. Cambridge University Press (UK).

CABI and EFSA resources used when preparing this datasheet

CABI Datasheet on Atropellis piniphila: https://www.cabi.org/isc/datasheet/7816 

Panel on Plant Health (PLH) Jeger M, Caffier D, Candresse T, Chatzivassiliou E, Dehnen‐Schmutz K et al. (2017) Pest risk assessment of Atropellis spp. for the EU territory. EFSA Journal 15(7), e04877. https://efsa.onlinelibrary.wiley.com/doi/full/10.2903/j.efsa.2017.4877

EFSA Panel on Plant Health (PLH) (2014) Scientific Opinion on the pest categorisation of Atropellis spp. EFSA Journal 12(12), 3926.

This datasheet was extensively revised in 2022 by Dr. Kateryna Davydenko, Ukrainian Research Institute of Forestry and Forest Melioration and Swedish University of Agricultural Science.  Her valuable contribution is gratefully acknowledged.

EPPO (2024) Atropellis piniphila. EPPO datasheets on pests recommended for regulation. https://gd.eppo.int (accessed 2024-04-20)

This datasheet was first published in the EPPO Bulletin in 1979 and revised in the two editions of 'Quarantine Pests for Europe' in 1992 and 1997, as well as in 2022. 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).

EPPO (1979) Data sheets on quarantine organisms No 5: Atropellis spp. EPPO Bulletin 9(2), 23-28. https://doi.org/10.1111/j.1365-2338.1979.tb02447.x