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. 2023 Jul 6;21(7):e08074. doi: 10.2903/j.efsa.2023.8074
Taxonomic information

Current valid scientific name: Entoleuca mammata

Synonyms: Anthostoma blakei, Anthostoma morsei, Fuckelia morsei, Hypoxylon blakei, Hypoxylon holwayi, Hypoxylon mammatum, Hypoxylon morsei, Hypoxylon pauperatum, Hypoxylon pruinatum, Nemania mammata, Rosellinia pruinata, Sphaeria mammata, Sphaeria pruinata (according to Index Fungorum)

Name used in the EU legislation: Entoleuca mammata (Wahlenb.) Rogers and Ju

Order: Xylariales

Family: Xylariaceae

Common name: hypoxylon canker of poplar, canker of aspen

Name used in the Dossier: Entoleuca mammata, Hypoxylon mammatum

Group Fungi
EPPO code HYPOMA
Regulated status

Entoleuca mammata is listed in Annex III of Commission Implementing Regulation (EU) 2019/2072 as protected zone quarantine pest for Ireland.

The pathogen is quarantine pest in China and Israel. It is on the A1 list of Türkiye (EPPO, online_a).

Pest status in the UK

Entoleuca mammata is present in the UK, with few occurrences in England, Wales, Channel Islands and Scotland (CABI, online; EPPO, online_b).

According to Dossier Section 5.0 the pathogen is present: not widely distributed and not under official control.

Pest status in the EU Entoleuca mammata is currently present in the EU in 19 MS: Austria, Belgium, Croatia, Czechia, Finland, France, Germany, Greece, Italy, Lithuania, the Netherlands, Slovakia, Slovenia, Sweden (EFSA PLH Panel, 2017); Denmark (GBIF, online); Estonia (Lutter et al., 2019) Latvia (Zeps et al., 2016); Poland and Spain (Farr and Rossman, online).
Host status on Acer

Entoleuca mammata was reported on Acer ginnala, A. rubrum, A. saccharum, A. saccarophorum and Acer sp. (Manion and Griffin, 1986; Farr and Rossman, online).

There is no information on whether Entoleuca mammata can also infect Acer pseudoplatanus.

PRA information Pest risk assessments available:
  • Scientific Opinion on the pest categorisation of Entoleuca mammata (EFSA PLH Panel, 2017);

  • UK risk register details for Entoleuca mammata (DEFRA, online);

  • Express pest risk analysis: Entoleuca mammata (Klejdysz et al., online).

Other relevant information for the assessment
Biology

Entoleuca mammata is an ascomycete fungus known as an important agent of canker disease in Populus species, mostly Populus tremuloides and P. tremula; other hardwood species like Salix spp. can also be infected (EFSA PLH Panel, 2017).

The pathogen is native to North America and was introduced into Europe several centuries ago (Kasanen et al., 2004); it is now largely spread in the temperate zones of the northern hemisphere. Entoleuca mammata is present in Canada and in some northern states of the US (Alaska, Iowa, Michigan, Minnesota, Montana, New Hampshire, New York, Wisconsin). In Europe, in addition to the 19 mentioned EU MS (see above), it is reported in Andorra, Bosnia and Herzegovina, Montenegro, North Macedonia, Russia (Southern Russia and Western Siberia) Serbia, Switzerland, Ukraine and the UK (CABI, online; EPPO, online_b) and Norway (NBIC, online).

The presence of E. mammata in Australia should be considered doubtful, as it is limited to a few specimens in herbarium without other records (EPPO, online_b).

The ascospores of E. mammata can infect the living wood of the hosts penetrating in the periderm and invading tissues under healthy bark and through mechanical wounds, as well as through injuries caused by woodpeckers and insects, in particular the North American cerambycid beetles (mostly Saperda inornata and Oberea spp.) (Anderson et al., 1979a) and the cicada Magicicada septendedecim (Ostry and Anderson, 1983) not occurring in Europe; water stress can increase host susceptibility (EFSA PLH Panel, 2017). Entoleuca mammata is mostly found on trees 15–40 years old, but all ages can be infected (EFSA PLH Panel, 2017; EPPO online_c). Infection usually starts from branches and twigs and then can spread to the main stem. The cankers expand very rapidly (7–8 cm per month) in summer and more slowly during winter; branches and stems can be girdled causing drying and breakage. The pathogen mostly develops in the range from 8 to 32°C, the optimum temperature is 28°C; toxins host‐specific produced by the fungus are involved in pathogenesis (Stermer et al., 1984; EFSA PLH Panel, 2017; EPPO, online_c).

Entoleuca mammata overwinters in host tissues as both mycelium and spores. 5 to 14 months after infection conidia are produced, but their role in the disease transmission is considered not relevant (EFSA PLH Panel, 2017).

The pathogen spreads over long distances via windborne ascospores, which are produced only 2–3 years after infection; cankers on felled trees on the ground can continue to produce ascospores for 23 months. Ascospores are dispersed with a temperature above −4°C and wet weather; a minimum of 16°C is required for starting germination, which became rapid at 28–32°C (EFSA PLH Panel, 2017).

Infected wood, mostly with bark, may be a pathway for passive spread of E. mammata in international trade; however, also young plants may carry ascospores or mycelium of the fungus, which can exist as a latent infection on living material inadvertently moved (EFSA PLH Panel, 2017; EPPO online_c).

Symptoms Main type of symptoms

The symptoms are observed on Populus trees. Early symptoms of cankers on the bark appear as slightly sunken, yellowish‐orange areas with an irregular border. Young cankers can be easily identified by removing the bark to expose the white mycelium in the cambial zone. The outer bark in older cankers is then lifted into blister‐like patches and break away, exposing blackened areas prominently visible on green branches and trunks. Callus formation only occasionally develops because cankers spread very quickly (Anderson et al., 1979b; EPPO, online_c).

Wilting of leaves may be observed when the trees are girdled, as well as sprouting of new shoots on stem and branches. Infected trees can be secondarily colonised by other fungi, accelerating the host decline (EPPO, online_c).

There is no information on the symptoms caused to Acer plants.

Presence of asymptomatic plants The disease caused by E. mammata has a latent period and symptoms can appear only 2 years after the ascospore infection; therefore, asymptomatic plants can be found (Ostry and Anderson, 2009).
Confusion with other pests

Some Hypoxylon species present in Europe on deciduous trees (H. confluens and H. udum) show symptoms similar to those of E. mammata but can be easily distinguished in laboratory by the ascospore characteris

tics (EFSA PLH Panel, 2017).

Host plant range

In North America, Entoleuca mammata mainly infects quacking aspen (Populus tremuloides); minor damage is recorded on P. grandidentata, P. balsamifera and various Populus hybrids.

Other secondary hosts in North America are Acer, Alnus, Betula, Carpinus, Fagus, Picea, Pyrus, Salix, Sorbus and Ulmus (Manion and Griffin, 1986).

In Europe, the main host is Populus tremula; other hosts are Populus alba, P. nigra, P. trichocarpa and the hybrid P. tremula x P. tremuloides (Ostry, 2013).

Reported evidence of impact

Entoleuca mammata is an important pathogen of poplars in the US and Canada, causing economic losses of millions of dollars a year (Anderson et al., 1979b; Ostry, 2013; EFSA PLH Panel, 2017). In Europe Entoleuca mammata is known as a pest of low importance, although damage on Populus tremula has been reported in France (Pinon, 1976), Italy and Sweden (EFSA PLH Panel, 2017).

Data on the incidence and impact of E. mammata on other woody species, Acer included, is not available and may be considered negligible.

Evidence that the commodity is a pathway Plants for planting may carry ascospores and mycelium of E. mammata also as asymptomatic plants (EFSA PLH Panel; EPPO online_c); therefore, the commodity is a pathway.
Surveillance information Entoleuca mammata is not a regulated pest for Great Britain and it is not under official control and surveillance in the UK (Dossier Sections 3.0 and 5.0).