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DOI: 10.2903/j.efsa.2024.8667
SCIENTIFIC OPINION
EFSA Panel on Plant Health (PLH) | Claude Bragard | Paula Baptista | Elisavet Chatzivassiliou |
Francesco Di Serio | Paolo Gonthier | Josep Anton Jaques Miret | Annemarie Fejer Justesen |
Alan MacLeod | Christer Sven Magnusson | Panagiotis Milonas | Juan A. Navas-Cortes |
Stephen Parnell | Roel Potting | Emilio Stefani | Hans-Hermann Thulke | Wopke Van der Werf |
Antonio Vicent Civera | Jonathan Yuen | Lucia Zappalà | Dejana Golic | Alex Gobbi |
Andrea Maiorano | Marco Pautasso | Philippe Lucien Reignault
Correspondence: plants@efsa.europa.eu
Abstract
Following the commodity risk assessment of bonsai plants (Pinus parviflora grafted
on Pinus thunbergii) from China performed by EFSA, the EFSA Plant Health Panel
performed a pest categorisation of Pyrrhoderma noxium, a clearly defined plant
pathogenic basidiomycete fungus of the order Hymenochaetales and the family
Hymenochaetaceae. The pathogen is considered as opportunistic and has been
reported on a wide range of hosts, mainly broad-leaved and coniferous woody
plants, causing root rots. In addition, the fungus was reported to live saprophyt-
ically on woody substrates and was isolated as an endophyte from a few plant
species. This pest categorisation focuses on the hosts that are relevant for the
EU (e.g. Citrus, Ficus, Pinus, Prunus, Pyrus, Quercus and Vitis vinifera). Pyrrhoderma
noxium is present in Africa, Central and South America, Asia and Oceania. It has
not been reported in the EU. Pyrrhoderma noxium is not included in Commission
Implementing Regulation (EU) 2019/2072. Plants for planting (excluding seeds),
bark and wood of host plants as well as soil and other growing media associated
with plant debris are the main pathways for the entry of the pathogen into the
EU. Host availability and climate suitability factors occurring in parts of the EU are
favourable for the establishment and spread of the pathogen. The introduction
and spread of the pathogen into the EU are expected to have an economic and en-
vironmental impact in parts of the territory where hosts are present. Phytosanitary
measures are available to prevent the introduction and spread of the pathogen
into the EU. Pyrrhoderma noxium satisfies all the criteria that are within the remit of
EFSA to assess for this species to be regarded as potential Union quarantine pest.
KEYWORDS
avocado, camellia, Diospyros, eucalyptus, Musa, Phellinus noxius, root rot
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© 2024 European Food Safety Authority. EFSA Journal published by Wiley-VCH GmbH on behalf of European Food Safety Authority.
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2 of 43 PYRRHODERMA NOXIUM: PEST CATEGORISATION
CO NTE NT S
Abstract�������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������1
1. Introduction��������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������4
1.1. Background and Terms of Reference as provided by the requestor�����������������������������������������������������������������������������������������4
1.1.1. Background������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������4
1.1.2. Terms of Reference����������������������������������������������������������������������������������������������������������������������������������������������������������������������4
1.2. Interpretation of the Terms of Reference��������������������������������������������������������������������������������������������������������������������������������������������4
1.3. Additional information������������������������������������������������������������������������������������������������������������������������������������������������������������������������������5
2. Data and methodologies��������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������5
2.1. Data�������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������5
2.1.1. Information on pest status from NPPOs������������������������������������������������������������������������������������������������������������������������������5
2.1.2. Literature search���������������������������������������������������������������������������������������������������������������������������������������������������������������������������5
2.1.3. Database search����������������������������������������������������������������������������������������������������������������������������������������������������������������������������5
2.2. Methodologies���������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������5
3. Pest Categorisation�������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������6
3.1. Identity and biology of the pest�������������������������������������������������������������������������������������������������������������������������������������������������������������6
3.1.1. Identity and taxonomy���������������������������������������������������������������������������������������������������������������������������������������������������������������6
3.1.2. Biology of the pest�����������������������������������������������������������������������������������������������������������������������������������������������������������������������7
3.1.3. Host range/species affected�����������������������������������������������������������������������������������������������������������������������������������������������������8
3.1.4. Intraspecific diversity������������������������������������������������������������������������������������������������������������������������������������������������������������������8
3.1.5. Detection and identification of the pest�����������������������������������������������������������������������������������������������������������������������������8
3.2. Pest distribution���������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������� 10
3.2.1. Pest distribution outside the EU������������������������������������������������������������������������������������������������������������������������������������������ 10
3.2.2. Pest distribution in the EU������������������������������������������������������������������������������������������������������������������������������������������������������ 10
3.3. Regulatory status�������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������� 10
3.3.1. Commission Implementing Regulation 2019/2072������������������������������������������������������������������������������������������������������� 10
3.3.2. Hosts or species affected that are prohibited from entering the union from third countries���������������������� 10
3.4. Entry, establishment and spread in the EU�������������������������������������������������������������������������������������������������������������������������������������� 12
3.4.1. Entry����������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������� 12
3.4.2. Establishment����������������������������������������������������������������������������������������������������������������������������������������������������������������������������� 13
3.4.2.1. EU distribution of main host plants������������������������������������������������������������������������������������������������������������������� 13
3.4.2.2. Climatic conditions affecting establishment������������������������������������������������������������������������������������������������� 13
3.4.3. Spread�������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������� 16
3.5. Impacts��������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������� 17
3.6. Available measures and their limitations����������������������������������������������������������������������������������������������������������������������������������������� 17
3.6.1. Identification of potential additional measures������������������������������������������������������������������������������������������������������������� 17
3.6.1.1. Additional potential risk reduction options��������������������������������������������������������������������������������������������������� 17
3.6.1.2. Additional supporting measures������������������������������������������������������������������������������������������������������������������������ 20
3.6.1.3. Biological or technical factors limiting the effectiveness of measures������������������������������������������������ 20
3.7. Uncertainty������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������� 20
4. Conclusions������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������� 21
Abbreviations����������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������� 21
Glossary���������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������� 21
Conflict of interest�������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������� 22
Requestor������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������� 22
Question number���������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������� 22
Copyright for non-EFSA content����������������������������������������������������������������������������������������������������������������������������������������������������������������������������� 22
Panel members�������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������� 22
References����������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������� 22
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PYRRHODERMA NOXIUM: PEST CATEGORISATION 3 of 43
Appendix A���������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������� 26
Appendix B���������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������� 37
Appendix C���������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������� 39
Appendix D���������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������� 43
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4 of 43 PYRRHODERMA NOXIUM: PEST CATEGORISATION
1.1.1 | Background
The new Plant Health Regulation (EU) 2016/2031, on the protective measures against pests of plants, is applying from 14
December 2019. Conditions are laid down in this legislation in order for pests to qualify for listing as Union quarantine pests,
protected zone quarantine pests or Union regulated non-quarantine pests. The lists of the EU regulated pests together
with the associated import or internal movement requirements of commodities are included in Commission Implementing
Regulation (EU) 2019/2072. Additionally, as stipulated in the Commission Implementing Regulation 2018/2019, certain com-
modities are provisionally prohibited to enter in the EU (high risk plants, HRP). EFSA is performing the risk assessment of the
dossiers submitted by exporting to the EU countries of the HRP commodities, as stipulated in Commission Implementing
Regulation 2018/2018. Furthermore, EFSA has evaluated a number of requests from exporting to the EU countries for dero-
gations from specific EU import requirements.
In line with the principles of the new plant health law, the European Commission with the Member States are discussing
monthly the reports of the interceptions and the outbreaks of pests notified by the Member States. Notifications of an im-
minent danger from pests that may fulfil the conditions for inclusion in the list of the Union quarantine pest are included.
Furthermore, EFSA has been performing horizon scanning of media and literature.
As a follow-up of the above-mentioned activities (reporting of interceptions and outbreaks, HRP, derogation requests
and horizon scanning), a number of pests of concern have been identified. EFSA is requested to provide scientific opinions
for these pests, in view of their potential inclusion by the risk manager in the lists of Commission Implementing Regulation
(EU) 2019/2072 and the inclusion of specific import requirements for relevant host commodities, when deemed necessary
by the risk manager.
EFSA is requested, pursuant to Article 29(1) of Regulation (EC) No 178/2002, to provide scientific opinions in the field of
plant health.
EFSA is requested to deliver 53 pest categorisations for the pests listed in Annex 1A, 1B, 1D and 1E (for more details see
mandate M-2021-00027 on the Open.EFSA portal). Additionally, EFSA is requested to perform pest categorisations for the
pests so far not regulated in the EU, identified as pests potentially associated with a commodity in the commodity risk as-
sessments of the HRP dossiers (Annex 1C; for more details see mandate M-2021-00027 on the Open.EFSA portal). Such pest
categorisations are needed in the case where there are not available risk assessments for the EU.
When the pests of Annex 1A are qualifying as potential Union quarantine pests, EFSA should proceed to phase 2 risk
assessment. The opinions should address entry pathways, spread, establishment, impact and include a risk reduction op-
tions analysis.
Additionally, EFSA is requested to develop further the quantitative methodology currently followed for risk assessment,
in order to have the possibility to deliver an express risk assessment methodology. Such methodological development
should take into account the EFSA Plant Health Panel Guidance on quantitative pest risk assessment and the experience
obtained during its implementation for the Union candidate priority pests and for the likelihood of pest freedom at entry
for the commodity risk assessment of High Risk Plants.
Phellinus noxius is one of a number of pests listed in Annex 1 to the Terms of Reference (ToR) to be subject to pest
categorisation to determine whether it fulfils the criteria of a potential Union quarantine pest for the area of the EU
excluding Ceuta, Melilla and the outermost regions of Member States referred to in Article 355(1) of the Treaty on the
Functioning of the European Union (TFEU), other than Madeira and the Azores, and so inform EU decision-making
as to its appropriateness for potential inclusion in the lists of pests of Commission Implementing Regulation (EU)
2019/2072. If a pest fulfils the criteria to be potentially listed as a Union quarantine pest, risk reduction options will be
identified.
Considering the nomenclature provided by Index Fungorum (https://www.indexfungorum.org/; accessed on 1
September 2023) according to which Pyrrhoderma noxium is the current name of Phellinus noxius on the basis of both mor-
phological and phylogenetic evidence (Zhou et al., 2018) (see Section 3.1.1 on Identity and Taxonomy), the Panel chose to
use the name Pyrrhoderma noxium instead of Phellinus noxius throughout the pest categorisation.
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PYRRHODERMA NOXIUM: PEST CATEGORISATION 5 of 43
This pest categorisation was initiated following the commodity risk assessment of bonsai plants (Pinus parviflora grafted
on Pinus thunbergii) from China performed by EFSA (EFSA PLH Panel, 2022), in which P. noxium was identified as a relevant
non-regulated EU pest, which could potentially enter the EU on bonsai plants.
2 | DATA AN D M E TH O DO LO G I ES
2.1 | Data
In the context of the current mandate, EFSA is preparing pest categorisations for new/emerging pests that are not yet regu-
lated in the EU. When official pest status is not available in the European and Mediterranean Plant Protection Organization
(EPPO) Global Database (EPPO, online), EFSA consults the NPPOs of the relevant MSs.
A literature search on P. noxium was conducted at the beginning of the categorisation in the ISI Web of Science biblio-
graphic database, using the scientific name of the pest as search term. Papers relevant for the pest categorisation were re-
viewed, and further references and information were obtained from experts, as well as from citations within the references
and grey literature. Pest information on hosts and distribution was retrieved through the systematic literature search, using
the EPPO Global Database and CABI (2022) as complementary sources.
Data about the import of commodity types that could potentially provide a pathway for the pest to enter the EU and about
the area of hosts grown in the EU were obtained from EUROSTAT (Statistical Office of the European Communities).
The Europhyt and TRACES databases were consulted for pest-specific notifications on interceptions and outbreaks.
Europhyt is a web-based network run by the Directorate General for Health and Food Safety (DG SANTÉ) of the European
Commission as a subproject of PHYSAN (Phyto-Sanitary Controls) specifically concerned with plant health information.
TRACES is the European Commission's multilingual online platform for sanitary and phytosanitary certification required
for the importation of animals, animal products, food and feed of non-animal origin and plants into the European Union,
and the intra-EU trade and EU exports of animals and certain animal products. Up until May 2020, the Europhyt database
managed notifications of interceptions of plants or plant products that do not comply with EU legislation, as well as notifi-
cations of plant pests detected in the territory of the Member States and the phytosanitary measures taken to eradicate or
avoid their spread. The recording of interceptions switched from Europhyt to TRACES in May 2020.
GenBank was searched to determine whether it contained any nucleotide sequences for P. noxium which could be used
as reference material for molecular diagnosis. GenBank® (www.ncbi.nlm.nih.gov/genbank/) is a comprehensive publicly
available database that as of August 2019 (release version 227) contained over 6.25 trillion base pairs from over 1.6 billion
nucleotide sequences for 450,000 formally described species (Sayers et al., 2020).
2.2 | Methodologies
The Panel performed the pest categorisation for P. noxium, following guiding principles and steps presented in the EFSA
guidance on quantitative pest risk assessment (EFSA PLH Panel, 2018), the EFSA guidance on the use of the weight of
evidence approach in scientific assessments (EFSA Scientific Committee, 2017) and the International Standards for
Phytosanitary Measures No. 11 (FAO, 2013).
The criteria to be considered when categorising a pest as a potential Union quarantine pest (QP) is given in Regulation
(EU) 2016/2031 Article 3 and Annex I, Section 1 of the Regulation. Table 1 presents the Regulation (EU) 2016/2031 pest cat-
egorisation criteria on which the Panel bases its conclusions. In judging whether a criterion is met the Panel uses its best
professional judgement (EFSA Scientific Committee, 2017) by integrating a range of evidence from a variety of sources (as
presented above in Section 2.1.) to reach an informed conclusion as to whether or not a criterion is satisfied.
The Panel's conclusions are formulated respecting its remit and particularly with regard to the principle of separation
between risk assessment and risk management (EFSA founding regulation (EU) No 178/2002); therefore, instead of deter-
mining whether the pest is likely to have an unacceptable impact, deemed to be a risk management decision, the Panel
will present a summary of the observed impacts in the areas where the pest occurs, and make a judgement about potential
likely impacts in the EU. While the Panel may quote impacts reported from areas where the pest occurs in monetary terms,
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6 of 43 PYRRHODERMA NOXIUM: PEST CATEGORISATION
the Panel will seek to express potential EU impacts in terms of yield and quality losses and not in monetary terms, in agree-
ment with the EFSA guidance on quantitative pest risk assessment (EFSA PLH Panel, 2018). Article 3 (d) of Regulation (EU)
2016/2031 refers to unacceptable social impact as a criterion for quarantine pest status. Assessing social impact is outside
the remit of the Panel.
T A B L E 1 Pest categorisation criteria under evaluation, as derived from Regulation (EU) 2016/2031 on protective measures against pests of plants
(the number of the relevant sections of the pest categorisation is shown in brackets in the first column).
Criterion of pest categorisation Criterion in Regulation (EU) 2016/2031 regarding union quarantine pest (article 3)
Identity of the pest (Section 3.1) Is the identity of the pest clearly defined, or has it been shown to produce consistent
symptoms and to be transmissible?
Absence/presence of the pest in the EU territory Is the pest present in the EU territory?
(Section 3.2) If present, is the pest in a limited part of the EU or is it scarce, irregular, isolated or present
infrequently? If so, the pest is considered to be not widely distributed.
Pest potential for entry, establishment and Is the pest able to enter into, become established in, and spread within, the EU territory? If
spread in the EU territory (Section 3.4) yes, briefly list the pathways for entry and spread.
Potential for consequences in the EU territory Would the pests' introduction have an economic or environmental impact on the EU
(Section 3.5) territory?
Available measures (Section 3.6) Are there measures available to prevent pest entry, establishment, spread or impacts?
Conclusion of pest categorisation (Section 4) A statement as to whether (1) all criteria assessed by EFSA above for consideration as a
potential quarantine pest were met and (2) if not, which one(s) were not met
Is the identity of the pest clearly defined, or has it been shown to produce consistent symptoms and/or to be
transmissible?
Yes, the identity of Pyrrhoderma noxium is clearly defined and the pathogen has been shown to produce consist-
ent symptoms and to be transmissible.
Pyrrhoderma noxium (Corner) L.W. Zhou & Y.C. Dai is a basidiomycete plant pathogenic fungus of the order Hymenochaetales
and family Hymenochaetaceae (Index Fungorum; accessed on 1 September 2023).
This pathogen was first described as Fomes noxius by Corner in 1932 (Corner, 1932). It was then renamed as Phellinus
noxius (Cunningham, 1965), which is the predominant name found in the literature, and thereafter as Phellinidium nox-
ium (Bondartseva et al., 1992). More recently, morphological and phylogenetic molecular analysis reassigned Phellinidium
noxium to the genus Pyrrhoderma, as Pyrrhoderma noxium (Zhou et al., 2018). Although this is the current name of the
fungus (Index Fungorum; accessed on 1 September 2023), the phylogeny and taxonomy of this species should be further
analysed (Stewart et al., 2020; Zhou et al., 2018). Indeed, recent phylogenetic analyses based on ITS (internal transcribed
spacer) and LSU (28S nuclear large sub-unit) rDNA genes suggest that Pyrrhoderma noxium may represent several distinct
genetic groups (Garfinkel et al., 2020). Moreover, Stewart et al. (2020) based on their phylogenetic study suggested that
Phellinus noxius isolates from eastern Asia and Oceania are distinct from Pyrrhoderma noxium and that Phellinus noxius may
represent one or more cryptic species. According to the same authors, these are preliminary results and further analyses
were recommended to better resolve P. noxium species boundaries. Indeed, the LSU and ITS markers used in the work of
Stewart et al. (2020) yield different clustering patterns, with the LSU showing a greater distinction between Phellinus noxius
and Pyrrhoderma noxium than the ITS marker, suggesting that further analyses are needed to better resolve P. noxium spe-
cies boundaries. The EPPO Global Database (EPPO, online) provides taxonomic identification only for the previous name
Phellinus noxius, as followed:
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PYRRHODERMA NOXIUM: PEST CATEGORISATION 7 of 43
Nevertheless, in this pest categorisation, the Panel adopted the nomenclature provided by Index Fungorum (https://
www.indexfungorum.org/; accessed on 1 September 2023) according to which Pyrrhoderma noxium is the current name of
Phellinus noxius on the basis of both morphological and phylogenetic evidence (Zhou et al., 2018). As explained in Section 1.2,
the Panel chose thus to use the name Pyrrhoderma noxium to refer to the pathogen throughout the pest categorisation.
Synonyms: Fomes noxius Corner (EPPO, online). Additional synonyms listed in Index Fungorum (accessed on 1 September
2023) include Phellinidium noxium (Corner) Bondartseva & S. Herrera, and Phellinus noxius (Corner) G. Cunn.
The EPPO code1 (EPPO, 2019; Griessinger & Roy, 2015) for this species is PHELNO (EPPO, online).
Pyrrhoderma noxium is a facultative pathogen that causes brown root-rot on a wide range of plant species, including mostly
woody species but also herbaceous ones (see Section 3.1.3). It can also live saprophytically on woody substrates in soil and
become a parasite when both favourable environmental conditions and hosts are present (Chang, 1996). In addition, this spe-
cies has been also isolated as an endophyte from a few plant species (Chen et al., 2011), including rice (Absalan et al., 2023).
Infected roots, stumps and woody debris in the soil are reported as the main source of inoculum for infection and as
substrates for the long-term (up to 10 years) survival of P. noxium (Chang, 1996). The fungus does not produce any long-
lived survival structures, such as chlamydospores (Chang, 1996), and it has limited ability to grow in the soil under field
conditions without the presence of woody plant debris (Wu et al., 2020). Therefore, soil without infected woody debris
cannot be considered as a long-term reservoir of P. noxium inoculum (Wu et al., 2020). Nevertheless, artificial inoculation
experiments showed that basidiospores, arthrospores (formed by fragmentation of the mycelium) and mycelia of P. noxium
can survive in soil up to 4.5 months, 3.5 months and 10 weeks, respectively (Chang, 1996).
Although both basidiospores and arthrospores are apparently not suitable structures for long-term survival, they may
play an important role in the long-distance dispersal of P. noxium via air currents (Chung et al., 2015). This role is mostly
ascribed to basidiospores (Chung et al., 2015), since arthrospores have never been observed in nature (Bolland, 1984), but
only in axenic culture (Leung et al., 2020; Sahashi et al., 2012). In contrast, basidiocarps and basidiospores of P. noxium have
been observed under natural conditions on dead and fallen trees (Chung et al., 2015; Hsiao et al., 2019). Basidiospores of P.
noxium can be produced on two different types of fructifications, a flat (resupinate) type and a bracket type, with the flat
type being the most frequently found in nature (Hsiao et al., 2019). In addition, these basidiospores can be disseminated
by wind (Cannon et al., 2022; Chung et al., 2015). Although the majority of basidiospores travel only few metres from the
basidiocarps, it is likely that the effective dispersal range of a low number of basidiospores can be higher, reaching several
kilometres (Chung et al., 2015). Basidiospores of P. noxium can directly infect stumps and lower stem/trunk (less than two
metres from the ground) through wounds (Ann et al., 2002; Bolland, 1984; Hsiao et al., 2019).
However, infections by means of P. noxium basidiospores can also occur indirectly by first germinating and colonising
plant debris in the soil, from which the mycelium grows to infect the lateral and taproots of a neighbouring host plant
(Ann et al., 2002; Chung et al., 2015). Indeed, the most common way of infection of P. noxium is either between roots of a
living tree and infected debris in the soil or root-to-root contact between infected trees and healthy adjacent ones (Ann
et al., 2002; Chung et al., 2015). Pyrrhoderma noxium can remain viable in fragments of contaminated roots up to 2 years,
and inside the root system of dead trees up to 10 years (Chang, 1996).
Infection by P. noxium usually begins in the roots. This fungus colonises the root system, grows towards the trunk and
covers the stem base and the root collar of the tree with a dark brown to blackish mycelial crust (Bolland, 1984). The growth
of this mycelial crust can reach heights up to 5 m, but it is more commonly found in the first 0.3–0.9 m from the tree trunk
base (Cannon et al., 2022). During the colonisation, P. noxium secretes enzymes that break down the cellulose, haemicel-
lulose and lignin in the woody root tissues, leading to the decay of the root structure (Cannon et al., 2022). This results in
a significant reduction in physical support and in disruption of the flow of water and nutrients to the tree, further leading
to its decline (Ann et al., 2002). Basidiocarps can develop on standing trees (bracket-like sporocarp) or trees blown down
(resupinate-like sporocarp) (Bolland, 1984), especially under warm and humid weather conditions (Wu et al., 2020). Both
basidiocarps produce airborne spores that can spread around and infect tree stumps and wounds in living trees, leading to
the establishment of new infection sites (Ann et al., 2002; Hsiao et al., 2019; Wu et al., 2020).
Plants of all ages are susceptible to P. noxium infection (Ann et al., 2002). Nevertheless, the progression of the disease is gen-
erally faster in young trees than in old ones (Gray, 2017). The time from the initial infection to the appearance of visible signs
and symptoms of the disease can vary widely depending on various factors, including the host plant species, environmental
conditions and virulence of P. noxium genotypes (Cannon et al., 2022). In most tree species, it takes 1–2 months from the initial
infection for symptoms to become apparent on the host, causing its death within 2–3 months (quick decline) (Ann et al., 2002;
Ann, Lee, & Tsai, 1999). However, in some cases, symptoms of P. noxium-caused brown root rot disease may occur over periods
of a year or more, generally culminating in tree death within 2–3 years (slow decline) (Ann et al., 2002; Ann, Lee, & Tsai, 1999).
In laboratory conditions, and in potato dextrose agar medium, P. noxium can grow at temperatures between 12°C and
36°C, with the optimal temperature near 30°C (Ann, Lee, & Huang, 1999), at which growth rate can reach 35 mm/day (Ann
1
An EPPO code, formerly known as a Bayer code, is a unique identifier linked to the name of a plant or plant pest important in agriculture and plant protection. Codes are
based on genus and species names. However, if a scientific name is changed, the EPPO code remains the same. This provides a harmonised system to facilitate the
management of plant and pest names in computerised databases, as well as data exchange between IT systems (EPPO, 2019; Griessinger & Roy, 2015).
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8 of 43 PYRRHODERMA NOXIUM: PEST CATEGORISATION
et al., 2002; Ann, Lee, & Huang, 1999). The fungus does not grow below 8°C or above 36°C (Ann, Lee, & Huang, 1999).
Pyrrhoderma noxium prefers acid soils, since it has been shown to grow at pH ranging from 3.5 to 7.0, whereas at pH above
7.5, its growth is inhibited in potato dextrose broth (Ann, Lee, & Huang, 1999).
Genomic and transcriptomic studies on P. noxium revealed that this pathogen has at least 488 genes that encode plant
cell wall-degrading enzymes, with slight differences on their expression during colonisation of different wood substrates
(Ibarra Caballero et al., 2020). According to the same authors, these genomic features of P. noxium might be responsible for
its wide host range and its capacity to quickly kill tree hosts.
Pyrrhoderma noxium is an opportunistic pathogen reported to infect a wide range of plant species (Ann, Lee, & Huang, 1999;
Chang, 1995b), including more than 430 species, from 246 genera and 85 families (Appendix A). The list of host plants encom-
passes mostly broad-leaved and coniferous woody species, and to a lesser extent herbaceous species (Appendix A). The most
diversified (with most genera) families among its host range are Fabaceae, Moraceae, Lauraceae, Malvaceae, Euphorbiaceae,
Myrtaceae, Meliaceae, Rosaceae, Arecaceae, Rubiaceae, Pinaceae and Rutaceae; while the most diversified (with most species)
genera are Ficus, Cinnamomum, Macaranga, Prunus, Acacia, Bauhinia, Eucalyptus, Citrus, Diospyros and Pinus.
As shown in Appendix A, P. noxium has been mostly associated with tropical and subtropical plant species. However,
P. noxium hosts also include many plant species with high relevance for the EU, namely Acacia spp. (Ann et al., 2002),
Bauhinia spp. (e.g. Ann et al., 2002), Citrus spp. (Stewart et al., 2020; Tsai et al., 2017), Camellia spp. (Ann et al., 2002), Diospyros
spp., including D. kaki (Ann et al., 2002; Ann, Lee, & Huang, 1999; Tsai et al., 2017), Eucalyptus spp. (Agustini et al., 2014; Ann
et al., 2002; Glen et al., 2014; Hsiao et al., 2019), Ficus spp. (Ann et al., 2002; Brooks, 2002; Gray, 2017; Hsiao et al., 2019; Tsai
et al., 2017), Musa spp. (Ivory & Daruhi, 1993; Stewart et al., 2020), Persea americana (Ann et al., 2002; Stewart et al., 2020),
Pinus spp. (Abe et al., 1995; Ann et al., 2002), Prunus spp., including P. armeniaca (Tsai et al., 2017) and P. persica (Akiba
et al., 2015; Ann et al., 2002; Tsai et al., 2017), Pyrus spp., including P. communis (Ann et al., 2002; Tsai et al., 2017), Quercus sp.
(Chung et al., 2015) and Vitis vinifera (Ann et al., 2002; Tsai et al., 2017).
Given that the symptoms of P. noxium in the belowground tree parts and lower stem are rather specific and distinct from
those of other root rot pathogens (see Section 3.1.5), there is less uncertainty about its host range than for other pathogens
where the identification of hosts cannot be based on visual symptoms and molecular methods are needed to confirm host
status (e.g. Pestalotiopsis microspora). However, it is likely that P. noxium can infect other plant species, given the ability of
this pathogen to produce a great variety of plant cell wall-degrading enzymes (see Section 3.1.2), and thus enhancing its
capacity to infect diverse hosts.
Different molecular techniques, such as DNA sequencing and genotyping, have been used to analyse the genetic diversity
within and among populations of P. noxium. All those studies found high levels of genetic diversity within populations. For
example, population genetic analyses of P. noxium isolates from Taiwan and Japan, using simple sequence repeat (SSR)
markers (Akiba et al., 2015; Chung et al., 2015) and whole-genome sequencing (Chung et al., 2017), revealed a high diversity
of genotypes at population level. Similarly, distinct lineages were identified within 95 P. noxium isolates from geographi-
cally diverse locations across eastern Asia and Oceania, based on sequences of four nuclear DNA loci (Stewart et al., 2020).
In contrast to the nuclear genome, the mitochondrial genome of P. noxium is nearly identical among isolates at protein-
coding regions, but differs greatly in the length of the non-coding regions (i.e. intergenic sequences) (Lee et al., 2019).
There is evidence of mitochondrial exchange between P. noxium individual fungal cells, possibly occurring during hy-
phal fusion and mating (Lee et al., 2019). This exchange of mitochondrial material may lead to the formation of recombinant
mitotypes (i.e. new combinations of mitochondrial DNA), potentially giving rise to novel genotypes (Lee et al., 2019). The
ability of P. noxium to reproduce sexually (Chung et al., 2015, 2017) can also contribute to the increase of genetic diversity
within populations. This may have implications on the plasticity and adaptation of the different P. noxium genotypes to var-
ious adverse environmental conditions, including fungicide exposure. It can also have important implications for P. noxium
virulence. Indeed, differences in virulence have been detected among isolates of P. noxium obtained from either the same
or from different host species (Nandris et al., 1987; Sahashi et al., 2010).
Yes, there are methods available for the detection and identification of Pyrrhoderma noxium.
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PYRRHODERMA NOXIUM: PEST CATEGORISATION 9 of 43
Pyrrhoderma noxium is a pathogen that primarily infects the root system of various tree species, causing brown root-rot
(Ann et al., 2002). Trees infected by P. noxium often exhibit reduced plant growth, yellowing and wilting of leaves, defolia-
tion, branch dieback, leading eventually to plant death within a few months (quick decline) to several years (slow decline)
(Ann et al., 2002; Ann, Lee, & Tsai, 1999; Sahashi et al., 2012). In general, young trees showed more rapid death than older
trees (Sahashi et al., 2012). However, these aboveground symptoms can vary greatly depending on the tree species, the
age and environmental conditions and are visible only at a later stage of infection (Sahashi et al., 2012). In addition, most of
those symptoms are similar to those caused by many root rot pathogens (Sahashi et al., 2012). In contrast, the symptoms of
P. noxium in the belowground tree parts and lower stem are rather specific and distinct from those of other root rot patho-
gens. They are typically characterised by a dark brown-blackish thick mycelial sheath or crust formed on the surface of the
roots and lower stem of infected trees (Sahashi et al., 2012). This crust/sheath may also have soil particles and small stones
stuck to it when P. noxium is growing in contact with soil (Sahashi et al., 2012). The internal root tissue is brown at first and
then turns white and soft, with a network of dark brown lines all over (Chung et al., 2015). In the advanced stages of decay,
a thin white to brown mycelial mat forms between the bark and wood (Sahashi et al., 2012). The presence of P. noxium ba-
sidiocarps on the basal trunk or exposed roots can also be a sign of brown root-rot disease (Cannon et al., 2022). However,
basidiocarps are not always present in natural conditions, especially during dry periods.
Morphology
Pyrrhoderma noxium can be easily isolated on culture media from roots or lower parts of basal stems exhibiting symptoms
(Sahashi et al., 2012). A selective medium for P. noxium was developed by Chang (1995a), using malt extract agar as a basal
medium amended with a set of antibiotics and fungicides. When growing in culture, P. noxium colonies exhibit certain
characteristics that may aid in its identification. In potato sucrose agar, the mycelial colonies are at first white, turning to
brown, with irregular dark brown lines or patches (Sahashi et al., 2012). In potato dextrose agar, the fungus produces brown
mycelial colonies with irregular dark brown lines or patches permeating the culture (Ann et al., 2002). Nevertheless, the ab-
sence of clamp connections formed during mitosis leading to mycelial growth and the presence of trichocysts (small, hair-
like projection on the surface of fungal cell) and arthrospores in culture are the main typical features of P. noxium (Figure 1)
(Ann, Lee, & Huang, 1999; Sahashi et al., 2012). Other species of Pyrrhoderma rarely produce arthrospores in culture (Chung
et al., 2015). On the other hand, on sawdust medium, P. noxium produces typical basidiocarps, after 3–4 months (Ann, Lee,
& Huang, 1999). They are thin (with about 0.5–2.0 cm thick), hard and uneven, first yellowish-brown with a white margin
and later become brown-dark grey (Ann et al., 2002; Ann, Lee, & Huang, 1999). Some morphological characteristics of the
hymenium and hyphal construction of the basidiocarp can also be used to distinguish P. noxium from its closely related
species Pyrrhoderma lamaoense (Ann et al., 2002). Pyrrhoderma noxium can be distinguished from P. lamaoense by hav-
ing wide setal hyphae (specialised structures distinguished from the vegetative hyphae mostly by thickened walls) and
the absence of setae (thick-walled cystidia) in the hymenium (see Figure 2 in Leung et al., 2020 for morphology pictures
of P. noxium examined by light microscopy and scanning electron microscopy) (Abe et al., 1995; Ann et al., 2002; Leung
et al., 2020). The basidiospores of P. noxium are smooth, hyaline and ovoid to broadly ellipsoid, averaging from 4.0 × 3.8
μm to 6.0 × 4.8 μm (Ann, Lee, & Huang, 1999). A more detailed morphological description of P. noxium is provided by Abe
et al. (1995) and CABI (2022).
DNA-based identification
The molecular techniques available for the identification of P. noxium are mostly based on the sequencing of the inter-
nal transcribed spacers (ITS) of genomic rDNA, in particular the region ITS1–5.8S–ITS2, the nuclear large subunit rDNA
(nrLSU) and protein-coding genes like the translation elongation factor 1-alpha (EF1-α) or the second largest subunits of
RNA polymerase II (RPB2) (Leung et al., 2020; Stewart et al., 2020; Tsai et al., 2017). As for other fungi, the combined use of
these genetic markers, often increase the accuracy of the identification and provides the resolution needed to separate P.
noxium from closely related species. Moreover, species-specific primers based on the ITS region of rDNA were developed
for P. noxium (Tsai et al., 2007; Wu et al., 2009). The presence and abundance of P. noxium in root tissues can also be evalu-
ated by quantitative real-time PCR (Liu et al., 2022) using the specific primers G1F (5’-GCCCTTTCCTCCGCTTATTG-3′) and
G1R2 (5’-ATTGGACTTGGGGACTGC-3′) targeting the ITS region (228 bp) developed by Wu et al. (2011). Nucleotide sequences
and whole genome of P. noxium are available in GenBank (www.ncbi.nlm.nih.gov/genbank; 815 sequences retrieved on 5
October 2023) and could be used as reference material for molecular diagnosis.
More recently, loop-mediated isothermal amplification (LAMP) was developed as a diagnostic tool to detect and iden-
tify P. noxium in culture (mycelium) and in wood chips (Zhang et al., 2022).
No EPPO Standard is available for the detection and identification of P. noxium.
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10 of 43 PYRRHODERMA NOXIUM: PEST CATEGORISATION
Pyrrhoderma noxium has been reported to be present in Central (Costa Rica, Cuba, Panama, Puerto Rico) and South America
(Brazil, Peru), Africa (Angola, Benin, Burkina Faso, Cameroon, Central African Republic, Chad, Democratic Republic of the
Congo, Gabon, Ghana, Guinea, Ivory Coast, Kenya, Liberia, Mali, Mauritania, Nigeria, Senegal, Sierra Leone, Tanzania, Togo,
and Uganda), Asia (China, Hong Kong, India, Indonesia, Japan, Malaysia, Myanmar, Pakistan, Philippines, Singapore, Sri
Lanka, Taiwan, Thailand, and Vietnam) and Oceania [American Samoa, Australia, Federated Stated of Micronesia (Chuuk,
Kosrae, Pohnpei, Yap), Fiji, French Polynesia, Guam, Mariana Island, Niue, Papua New Guinea, Republic of Palau, Republic of
Vanuatu, Rota Island, Saipan, Samoa and Solomon Islands]. The current geographical distribution of P. noxium is shown in
Figure 1. A list of the countries and states/provinces from where the fungus has been reported is included in Appendix B.
The records are based on the systematic literature search (Section 2.1.2), including information from CABI (2022).
FIGURE 1 Global distribution of Pyrrhoderma noxium. Sources: systematic literature review (Section 2.1.2) and CABI (2022) (see Appendix B).
Is the pest present in the EU territory? If present, is the pest in a limited part of the EU or is it scarce, irregular, isolated or
present infrequently? If so, the pest is considered to be not widely distributed.
Pyrrhoderma noxium is not listed in Annex II of Commission Implementing Regulation (EU) 2019/2072, an implementing act
of Regulation (EU) 2016/2031, or in any emergency plant health legislation.
3.3.2 | Hosts or species affected that are prohibited from entering the union from third countries
A list of commodities included in Annex VI of Commission Implementing Regulation (EU) 2019/2072 is provided in Table 2.
Some of the hosts relevant to the EU, Persea americana, Diospyros spp., Prunus spp. and Quercus spp., are included in the
Commission Implementing Regulation (EU) 2018/2019 on high-risk plants.
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PYRRHODERMA NOXIUM: PEST CATEGORISATION 11 of 43
T A B L E 2 List of plants, plant products and other objects that are Pyrrhoderma noxium hosts whose introduction into the Union from certain third
countries is prohibited (Source: Commission Implementing Regulation (EU) 2019/2072, Annex VI).
List of plants, plant products and other objects whose introduction into the union from certain third countries is prohibited
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12 of 43 PYRRHODERMA NOXIUM: PEST CATEGORISATION
3.4.1 | Entry
Is the pest able to enter into the EU territory? If yes, identify and list the pathways.
Yes. Pyrrhoderma noxium could potentially enter the EU, mainly via host plants for planting (excluding seeds for
sowing), parts of host plants (e.g. branches, bark, wood), and soil/plant growing media associated with debris of
host plants.
Plants for planting are a main pathway of entry of the pathogen into the EU.
The Panel identified the following main pathways for the entry of P. noxium into the EU territory:
Pyrrhoderma noxium is reported to infect the roots, base stem/trunk and root collar of plants (Section 3.1.2 Biology of
the pest). Thus, the pathogen could potentially enter into the EU territory on plant parts (e.g. stems). However, this is con-
sidered a minor pathway for the entry of the pathogen into the EU.
Although there are no data available, basidiospores (and arthrospores if they are produced in natural conditions) of the
pathogen may also be present as contaminants on other substrates or objects (e.g. second hand agricultural machinery
and equipment, crates, fresh fruit, etc.) imported into the EU from infested countries. Nevertheless, these are considered
minor pathways for the entry of the pathogen into the EU.
A list of all the potential pathways for the entry of the pathogen into the EU is included in Table 3.
The quantity of fresh produce of main hosts imported into the EU from countries where P. noxium is present is provided
in Table 4.
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PYRRHODERMA NOXIUM: PEST CATEGORISATION 13 of 43
T A B L E 4 EU annual imports of fresh produce of main hosts from countries where P. noxium is present, 2016–2020 (in 100 kg) Source: Eurostat,
accessed November 2023.
Notifications of interceptions of harmful organisms began to be compiled in Europhyt in May 1994 and in TRACES in May
2020. As of Nov 2023, there were no record of interception of Pyrrhoderma noxium in the Europhyt and TRACES databases.
3.4.2 | Establishment
Yes. Both the biotic (host availability) and abiotic (climate suitability) factors occurring in the EU suggest that P.
noxium could establish in parts of the EU where hosts are grown.
Following its entry into the EU, P. noxium could establish in parts of the EU where hosts are grown and the climatic conditions
are conducive to completing its life cycle. Based on its biology (see Section 3.1.2), P. noxium could potentially be transferred
from the pathways of entry to the host plants grown in the EU by root-to-root contact, wind, water (irrigation, rain) splash, soil or
other plant-growing media associated with infected plant debris, and possibly insects, as well as with birds and small mammals
(see Section 3.4.3). The frequency of this transfer depends on the volume and frequency of the imported commodities, their
destination (e.g. nurseries, retailers, packinghouses) and proximity to the hosts, as well as on the management of plant debris.
Climatic mapping is the principal method for identifying areas that could provide suitable conditions for the establish-
ment of a pest taking key abiotic factors into account (Baker, 2002). Availability of hosts is considered in Section 3.4.2.1.
Climatic factors are considered in Section 3.4.2.2.
TA B L E 5 Harvested area of some Pyrrhoderma noxium hosts relevant for the EU, 2017–2021 (1000 ha). Source: EUROSTAT (accessed November
2023).
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14 of 43 PYRRHODERMA NOXIUM: PEST CATEGORISATION
Regarding the interpretation of the soil temperature map, it should be kept in mind that:
• P. noxium is not a strict soilborne pathogen (freely living in the soil), but it is rather associated with plant/wood debris
incorporated in the soil;
• The temperature data refer to the top layer of soil (0–7 cm), while most ot the roots of trees, and therefore pathogen
inoculum, are expected to be present deeper in the soil, where temperatures may be different;
• Mycelial growth temperatures could be important to estimate the likelihood of establishment in this case (e.g. root-to-
root transmission), but temperatures allowing the development of fruiting bodies and sporulation would be even more
important. However, in this last case, the air temperature rather than the soil temperature would play a role, but this
could be covered by the hardiness zone map (Figure 3).
F I G U R E 2 Hardiness zone map based on the average annual minimum temperature for the period 1993–2022. The map highlights the hardiness
zones in Europe and some neighbouring areas where the average minimum temperature is higher or equal to the minimum value sampled using the
pathogen occurrence. This value is included in the hardiness zones ≥ 10a (highlighted in grey in the legend). The map is based on the implementation
of the USDA Plant Hardiness Zones (USDA, 2023).
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15 of 43
F I G U R E 3 Average total number of days with average soil temperature (0–7 cm) between 12°C and 36°C for Europe and neighbouring areas, with
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days in seven classes. Data Source: Muñoz-Sabater et al. (2021). Based on the 1993–2022 period.
PYRRHODERMA NOXIUM: PEST CATEGORISATION
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16 of 43 PYRRHODERMA NOXIUM: PEST CATEGORISATION
F I G U R E 4 Average total number of days with average soil temperature (0–7 cm) between 12°C and 36°C including only the areas in Europe and
neighbouring areas that have average total number of days greater than a threshold of 315 days, obtained from the points of observation. Same
data source as Figure 4. Please note that the pest distribution locations from remote islands may not have available information for soil temperature
(0–7 cm). This may have an effect on the threshold extracted for this pest.
3.4.3 | Spread
Describe how the pest would be able to spread within the EU territory following establishment.
Following its establishment in the EU, Pyrrhoderma noxium could potentially spread within the EU by both natural
and human-assisted means.
Host plants for planting are a main means of spread of P. noxium within the EU.
Pyrrhoderma noxium could potentially spread within the EU by natural and human-assisted means.
Spread by natural means. The rate of root-to-root spread of P. noxium is variable. Under optimal climatic conditions
(warm temperature and wet weather), a growth of 6 m per year of the mycelium along a row of susceptible trees is re-
ported (Cannon et al., 2022). This growth rate is likely to be lower under dry conditions and on resistant host trees (Cannon
et al., 2022). The survival and short-distance dispersion of P. noxium depends on infected plant tissues in the soil close to
host plants; while basidiospores are more likely to be involved in long-distance dispersal of the fungus (Hsiao et al., 2019).
Although it has not been studied in the case of P. noxium, wind, wind-driven rain, insects and small animals may also con-
tribute to the dispersal of basidiospores and arthrospores.
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PYRRHODERMA NOXIUM: PEST CATEGORISATION 17 of 43
Spread by human-assisted means. The pathogen can spread over long distances through the movement of infected
host plants for planting (e.g. rootstocks, grafted plants, scions), including dormant plants, as well as contaminated soil/
plant-growing media associated with plant debris and agricultural machinery, tools, etc. Similarly, infected wood (e.g.
timber, logs, sawdust) and wooden components (e.g. pallets), can serve as potential carriers for the spread of P. noxium
(Cannon et al., 2022).
3.5 | Impacts
Would the pests' introduction have an economic or environmental impact on the EU territory?
Yes, the introduction into and spread within the EU of Pyrrhoderma noxium is expected to have economic and
environmental impacts where hosts are grown.
The brown root rot caused by P. noxium has been reported as one of the most serious diseases of trees in the tropics and
subtropics (Ann et al., 2002). Indeed, P. noxium is a destructive and fast-growing pathogen that frequently causes rapid
death of a wide range of woody species (Cannon et al., 2022). In Japan, up to 41% tree mortality/decline due to P. noxium
was recorded in plantations, encompassing mostly Casuarina equisetifolia, Calophyllum inophyllum, Podocarpus macrophyl-
lus, Garcinia subelliptica, Delonix regia and Erythrina variegata (Abe et al., 1995). In the Ivory Coast, rubber tree (Hevea brasil-
iensis) plantations, around 25% incidence of trees infected by P. noxium was reported, with 63% mortality (Nandris
et al., 1988). Severe P. noxium damage on several woody tree species has also been reported from Taiwan (Chang, 1995b),
Mariana Islands (Hodges & Tenorio, 1984), Malaysia (Farid et al., 2005, 2009) and Australia (Bolland, 1984).
Besides plantations and native forest trees, P. noxium also caused significant yield losses in some fruit crop species. For
example, in avocado (Persea americana) orchards in Taiwan (Ann et al., 2002) and Australia (Dann et al., 2009), P. noxium was
reported to cause considerable losses to avocado growers by killing the trees. In Australia, there are reports of mortality rate
of 10% in several avocado orchards, with an estimated economic loss of $AUD5400 per hectare (Dann et al., 2009; Everett
& Siebert, 2018). Moreover, P. noxium can persist in the soil, even after infected plants are removed (see Section 3.1.2). This
long-term presence in the environment can continue to affect subsequent crops, leading to continuing yield losses if not
properly managed. In tropical countries where P. noxium has been noticed for a long time, it has established a reputation
of being a very aggressive pathogen (e.g. Ann, Lee, & Huang, 1999; Chang, 1995b; Farid et al., 2009).
Based on the above, it is expected that the introduction into and spread within the EU of P. noxium would potentially
have an economic and environmental impact where hosts are grown. Damage in those areas may be significant with
mortality of established trees, and failure of replanting. Pyrrhoderma noxium is a polyphagous pathogen (Ann, Lee, &
Huang, 1999; Chang, 1995b), so it may infect many plant species growing in the EU, whose susceptibility to P. noxium is
unknown. Should these species be suitable hosts of P. noxium, the economic and environmental impacts are likely to be
high as the pathogen can kill host plants.
Are there measures available to prevent pest entry, establishment, spread or impacts such that the risk becomes
mitigated?
Yes. Although not specifically targeted against Pyrrhoderma noxium, existing phytosanitary measures (see
Sections 3.3.2 and 3.4.1) mitigate the likelihood of the pathogen's entry into the EU territory on certain host plants.
Potential additional measures are also available to further mitigate the risk of entry, establishment, spread and
impacts of the pathogen in the EU (see Section 3.6.1).
Phytosanitary measures (prohibitions) are currently applied to some host plants for planting (see Section 3.3.2).
Additional potential risk reduction options and supporting measures are shown in Sections 3.6.1.1 and 3.6.1.2.
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18 of 43 PYRRHODERMA NOXIUM: PEST CATEGORISATION
T A B L E 6 Selected control measures (a full list is available in EFSA PLH Panel, 2018) for pest entry/establishment/spread/impact in relation to
currently unregulated hosts and pathways. Control measures are measures that have a direct effect on pest abundance.
Control measure/risk
reduction option Risk element targeted
(Blue underline = Zenodo (entry/establishment/
doc, Blue = WIP) RRO summary spread/impact)
Require pest freedom Plants, plant products and other objects must come from a pest-free country or Entry/Spread
a pest-free area or a pest-free place of production
Growing plants in isolation Description of possible exclusion conditions that could be implemented Entry/Establishment/
to isolate the crop from pests and if applicable relevant vectors. E.g. a Spread
dedicated structure such as glass or plastic greenhouses
Growing nursery plants in isolation may represent an effective control measure
Managed growing conditions Proper field drainage, plant distancing, use of pathogen-free agricultural tools Entry/Spread/Impact
(e.g. pruning scissors, saws and grafting blades), and removal of infected
plants and plant debris in the nursery/field/orchard could potentially
mitigate the likelihood of infection at origin as well as the spread of the
pathogen
Crop rotation, associations Crop rotation, associations and density, weed/volunteer control are used Establishment/Spread/
and density, weed/ to prevent problems related to pests and are usually applied in various Impact
volunteer control combinations to make the habitat less favourable for pests
The measures deal with (1) allocation of crops to field (over time and space)
(multi-crop, diversity cropping) and (2) to control weeds and volunteers as
hosts of pests/vectors
Although P. noxium has been isolated either as an endophyte or as a pathogen
from a wide range of hosts (Appendix A), crop rotation (wherever feasible)
may represent an effective means to reduce inoculum sources and potential
survival of the pathogen (Ann et al., 2002)
Use of resistant and tolerant Resistant plants are used to restrict the growth and development of a specified Entry/Establishment/
plant species/varieties pest and/or the damage they cause when compared to susceptible plant Impact
varieties under similar environmental conditions and pest pressure
• It is important to distinguish resistant from tolerant species/varieties
An approach to control root rot induced by P. noxium is to replant the infested
areas with resistant species (Ann, Lee, & Huang, 1999)
Roguing and pruning Roguing is defined as the removal of infested plants and/or uninfested host Entry/Spread/Impact
plants in a delimited area, whereas pruning is defined as the removal of
infested plant parts only without affecting the viability of the plant.
P. noxium survives as a saprophyte or colonises as an endophyte infected
attached plant organs, which can act as inoculum sources. Thus, roguing of
host plants may be an effective measure for reducing the inoculum sources
and the spread capacity of the pathogen in the field
Biological control, Biological control of P. noxium has been investigated at the laboratory scale Entry/Impact
Biopesticides and only on leaf oils obtained from the plant Cinnamomum osmophloeum
behavioural manipulation (Cheng et al., 2018), antagonistic fungi such as Trichoderma asperellum
(Chou et al., 2019), bacteria such as Streptomyces sp. and Bacillus sp. (Leung
et al., 2020)
The potential for biocontrol in the rhizosphere has been demonstrated,
particularly with species of Trichoderma (Jacob et al., 1991; Kothandaraman
et al., 1991)
Chemical treatments on crops Various fungicides have been found to have activity against the pathogen (Lim Entry/Establishment/
including reproductive et al., 1990; Mappes and Hiepko, 1984), but routine field treatments with Impact
material these fungicides are not economical
Chemical treatments on Use of chemical compounds that may be applied to plants or to plant products Entry/Spread
consignments or during after harvest, during process or packaging operations and storage
processing The treatments addressed in this information sheet are:
a. fumigation;
b. spraying/dipping pesticides;
c. surface disinfectants;
d. process additives;
e. protective compounds
As an example, the treatment of pallets can be mentioned
Physical treatments on This information sheet deals with the following categories of physical Entry/Spread
consignments or during treatments: irradiation/ionisation; mechanical cleaning (brushing, washing);
processing sorting and grading, and; removal of plant parts (e.g. debarking wood). This
information sheet does not address: heat and cold treatment (information
sheet 1.14); roguing and pruning (information sheet 1.12)
Physical treatments (irradiation, mechanical cleaning, sorting, etc.) may reduce
or mitigate the risk of entry/spread of P. noxium although no specific
information is available for this fungal species
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PYRRHODERMA NOXIUM: PEST CATEGORISATION 19 of 43
TA B L E 6 (Continued)
Control measure/risk
reduction option Risk element targeted
(Blue underline = Zenodo (entry/establishment/
doc, Blue = WIP) RRO summary spread/impact)
Cleaning and disinfection The physical and chemical cleaning and disinfection of facilities, tools, Entry/Spread
of facilities, tools and machinery, transport means, facilities and other accessories (e.g. boxes,
machinery pots, pallets, palox, supports, hand tools). The measures addressed in this
information sheet are washing, sweeping and fumigation
P. noxium infects its host plants mostly through contact of the inoculum with
roots. Therefore, and although no specific information is available on this
species, cleaning and surface sterilisation of soil tilling tools as well as
of equipment and facilities (including premises, storage areas) are good
cultural and handling practices employed in the production and marketing
of any commodity and may mitigate the likelihood of entry or spread of the
pathogen
Limits on soil P. noxium survives in the soil and on plant debris in or on the soil surface. Entry/Spread
Therefore, plants, plant products and other objects (e.g. used farm
machinery) should be free from soil to ensure freedom from P. noxium
Soil treatment The control of soil organisms by chemical and physical methods listed below: Entry/Establishment/
a. Fumigation; Impact
b. Heating;
c. Solarisation;
d. Flooding;
e. Soil suppression;
f. Augmentative Biological control;
g. Biofumigation
Many soil treatments have been tested and numerous experiments have been
performed to find an effective way of eliminating such inoculum. Currently,
the most efficient method of destroying the residual inoculum is by flooding
the field, and the most practical way is to fumigate the infested soil with
ammonia generated from urea amended in soil under alkaline conditions
(Ann and Ko, 1994; Chang, 1996; Chang & Chang, 1999)
Use of non-contaminated Chemical and physical treatment of water to eliminate waterborne Entry/Spread
water microorganisms. The measures addressed in this information sheet are
chemical treatments (e.g. chlorine, chlorine dioxide, ozone); physical
treatments (e.g. membrane filters, ultraviolet radiation, heat); ecological
treatments (e.g. slow sand filtration)
Considering that P. noxium may spread via contaminated irrigation water,
physical or chemical treatment of irrigation water may be applied in
nurseries and greenhouses. However, also disinfected water, once used to
clean plant material, can transfer inoculum from a source to other plants
Waste management • Treatment of the waste (deep burial, composting, incineration, chipping, Establishment/Spread
production of bio-energy…) in authorised facilities and official restriction on
the movement of waste.
Waste management in authorised facilities and official restriction on its
movement may prevent the pathogen from escaping in the environment.
On-site proper management of roguing residues is also recommended as an
efficient measure
Heat and cold treatments Controlled temperature treatments aimed to kill or inactivate pests without Entry/Spread
causing any unacceptable prejudice to the treated material itself. The
measures addressed in this information sheet are autoclaving; steam; hot
water; hot air; cold treatment
In laboratory conditions, the fungus does not grow below 8°C or above 36°C
(Ann, Lee, & Huang, 1999). Kiln drying of wood and heat treatment of pallets
are relevant measures here, although specific data on effectiveness against
P. noxium are lacking
Conditions of transport Specific requirements for mode and timing of transport of commodities to Entry/Spread
prevent escape of the pest and/or contamination.
a. Physical protection of consignment
b. Timing of transport/trade
If plant material, potentially infected or contaminated with P. noxium (including
waste material) must be transported, specific transport conditions (type of
packaging/protection, transport means) should be defined to prevent the
pathogen from escaping. These may include, albeit not exclusively: physical
protection, sorting prior to transport, sealed packaging, etc.
(Continues)
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20 of 43 PYRRHODERMA NOXIUM: PEST CATEGORISATION
TA B L E 6 (Continued)
Control measure/risk
reduction option Risk element targeted
(Blue underline = Zenodo (entry/establishment/
doc, Blue = WIP) RRO summary spread/impact)
Post-entry quarantine This information sheet covers post-entry quarantine (PEQ) of relevant Establishment/Spread
and other restrictions commodities; temporal, spatial and end-use restrictions in the importing
of movement in the country for import of relevant commodities; Prohibition of import of
importing country relevant commodities into the domestic country
‘Relevant commodities’ are plants, plant parts and other materials that may
carry pests, either as infection, infestation or contamination
Recommended for plant species known to be hosts of P. noxium. This measure
does not apply to fruits of host plants
T A B L E 7 Selected supporting measures (a full list is available in EFSA PLH Panel, 2018) in relation to currently unregulated hosts and pathways.
Supporting measures are organisational measures or procedures supporting the choice of appropriate risk reduction options that do not directly
affect pest abundance.
3.7 | Uncertainty
No key uncertainty was identified.
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PYRRHODERMA NOXIUM: PEST CATEGORISATION 21 of 43
4 | CO NCLUSIO NS
Pyrrhoderma noxium satisfies all the criteria that are within the remit of EFSA to assess for this species to be regarded as
potential Union quarantine pest (Table 8).
T A B L E 8 The Panel's conclusions on the pest categorisation criteria defined in Regulation (EU) 2016/2031 on protective measures against pests of
plants (the number of the relevant sections of the pest categorisation is shown in brackets in the first column).
A B B R E V I AT I O N S
EPPO European and Mediterranean Plant Protection Organization
FAO Food and Agriculture Organization
HRP high-risk plants
IPPC International Plant Protection Convention
ISPM International Standards for Phytosanitary Measures
MS Member State
PLH EFSA Panel on Plant Health
PZ Protected Zone
TFEU Treaty on the Functioning of the European Union
ToR Terms of Reference
GLOSSARY
Containment (of a pest) Application of phytosanitary measures in and around an infested area to prevent spread of
a pest (FAO, 2022).
Control (of a pest) Suppression, containment or eradication of a pest population (FAO, 2022).
Entry (of a pest) Movement of a pest into an area where it is not yet present, or present but not widely dis-
tributed and being officially controlled (FAO, 2022).
Eradication (of a pest) Application of phytosanitary measures to eliminate a pest from an area (FAO, 2022).
Establishment (of a pest) Perpetuation, for the foreseeable future, of a pest within an area after entry (FAO, 2022).
Greenhouse A walk-in, static, closed place of crop production with a usually translucent outer shell,
which allows controlled exchange of material and energy with the surroundings and pre-
vents release of plant protection products (PPPs) into the environment.
Hitchhiker An organism sheltering or transported accidentally via inanimate pathways including with
machinery, shipping containers and vehicles; such organisms are also known as contami-
nating pests or stowaways (Toy & Newfield, 2010).
Impact (of a pest) The impact of the pest on the crop output and quality and on the environment in the oc-
cupied spatial units.
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22 of 43 PYRRHODERMA NOXIUM: PEST CATEGORISATION
Introduction (of a pest) The entry of a pest resulting in its establishment (FAO, 2022).
Pathway Any means that allows the entry or spread of a pest (FAO, 2022).
Phytosanitary measures Any legislation, regulation or official procedure having the purpose to prevent the intro-
duction or spread of quarantine pests, or to limit the economic impact of regulated non-
quarantine pests (FAO, 2022).
Quarantine pest A pest of potential economic importance to the area endangered thereby and not yet pre-
sent there, or present but not widely distributed and being officially controlled (FAO, 2022).
Risk reduction option (RRO) A measure acting on pest introduction and/or pest spread and/or the magnitude of the
biological impact of the pest should the pest be present. A RRO may become a phytosani-
tary measure, action or procedure according to the decision of the risk manager.
Spread (of a pest) Expansion of the geographical distribution of a pest within an area (FAO, 2022).
CONFLIC T OF INTEREST
If you wish to access the declaration of interests of any expert contributing to an EFSA scientific assessment, please contact
interestmanagement@efsa.europa.eu.
REQUESTOR
European Commission
QUESTION NUMBER
EFSA-Q -2024-00349
MAP DISCLAIMER
The designations employed and the presentation of material on any maps included in this scientific output do not imply
the expression of any opinion whatsoever on the part of the European Food Safety Authority concerning the legal status of
any country, territory, city or area or of its authorities, or concerning the delimitation of its frontiers or boundaries.
C O P Y R I G H T F O R N O N - E F S A C O N T E N T
EFSA may include images or other content for which it does not hold copyright. In such cases, EFSA indicates the copyright
holder and users should seek permission to reproduce the content from the original source.
PA N E L M E M B E R S
Claude Bragard, Paula Baptista, Elisavet Chatzivassiliou, Francesco Di Serio, Paolo Gonthier, Josep Anton Jaques Miret,
Annemarie Fejer Justesen, Alan MacLeod, Christer Sven Magnusson, Panagiotis Milonas, Juan A. Navas-Cortes, Stephen
Parnell, Roel Potting, Philippe L. Reignault, Emilio Stefani, Hans-Hermann Thulke, Wopke Van der Werf, Antonio Vicent
Civera, Jonathan Yuen, and Lucia Zappalà.
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Wang, Y.-F., Meng, H., Gu, V. W., & Gu, J.-D. (2016). Molecular diagnosis of the brown root rot disease agent Phellinus noxius on trees and in soil by rDNA
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Wu, J., Peng, S. L., Zhao, H. B., Tang, M. H., Li, F. R., & Chen, B. M. (2011). Selection of species resistant to the wood rot fungus Phellinus noxius. European
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How to cite this article: EFSA PLH Panel (EFSA Panel on Plant Health), Bragard, C., Baptista, P., Chatzivassiliou, E., Di
Serio, F., Gonthier, P., Jaques Miret, J. A., Justesen, A. F., MacLeod, A., Magnusson, C. S., Milonas, P., Navas-Cortes, J. A.,
Parnell, S., Potting, R., Stefani, E., Thulke, H.-H., Van der Werf, W., Vicent Civera, A., Yuen, J., Zappalà, L. … Reignault, P.
L. (2024). Pest categorisation of Pyrrhoderma noxium. EFSA Journal, 22(3), e8667. https://doi.org/10.2903/j.
efsa.2024.8667
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26 of 43 PYRRHODERMA NOXIUM: PEST CATEGORISATION
APPE N D IX A
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PYRRHODERMA NOXIUM: PEST CATEGORISATION 27 of 43
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PYRRHODERMA NOXIUM: PEST CATEGORISATION 29 of 43
(Continues)
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PYRRHODERMA NOXIUM: PEST CATEGORISATION 31 of 43
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PYRRHODERMA NOXIUM: PEST CATEGORISATION 33 of 43
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PYRRHODERMA NOXIUM: PEST CATEGORISATION 35 of 43
(Continues)
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36 of 43 PYRRHODERMA NOXIUM: PEST CATEGORISATION
Lactuca indica Asteraceae Wild lettuce Chang and Yang (1998), Ann
et al. (2002)
Melicope merrilli Rutaceae Melicope Ann et al. (2002)
Oplismenus compositus Poaceae Basket grass Chen et al. (2023)
Paspalum distichum Poaceae Chen et al. (2023)
Saurauia oldhamii (Syn. Actinidiaceae Ann et al. (2002)
Saurauia tristyla)
Typhonium blumei Araceae Chen et al. (2023)
Urena lobata Malvaceae Cadillo Ann et al. (2002)
Zoysia matrella Poaceae Manila grass Chen et al. (2023)
Artificial/ Calophyllum vexans Calophyllaceae Abe et al. (1995)
experimental
host
Cassia bicapsularis (Syn. Senna Fabaceae Christmas bush Ann, Tsai, Wang, and Hsien (1999)
bicapsularis)
Citrus grandis (Syn. Citrus Rutaceae Pampelmuse Ann, Tsai, Wang, and Hsien (1999)
maxima)
Citrus reticulata Rutaceae Mandarin orange Ann, Tsai, Wang, and Hsien (1999)
Citrus sinensis Rutaceae Sweet orange Ann, Tsai, Wang, and Hsien (1999)
Euphoria longana (Syn. Sapindaceae Longan Ann, Lee, and Huang (1999)
Dimocarpus longan)
Fagus crenata Fagaceae Siebold’s beech, Japanese Abe et al. (1995)
beech
Jasminum sambac Oleaceae Arabian jasmine Ann, Tsai, Wang, and Hsien (1999)
Paspalum conjugatum Poaceae Chen et al. (2023)
Quercus acutissima Fagaceae Abe et al. (1995)
Thespesia populnea Malvaceae Portia tree Hodges and Tenorio (1984)
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PYRRHODERMA NOXIUM: PEST CATEGORISATION 37 of 43
APPE N D IX B
Sub-national (e.g.
Region Country state) Status References
North America Cuba Present, no details CABI (2022)
Puerto Rico Present, no details CABI (2022)
Central America Costa Rica Present, no details CABI (2022)
Panama Present, no details Zhou et al. (2018)
South America Brazil Present, no details Mendes & Urben (2023)
Peru Present, no details CABI (1969)
Africa Angola Present, no details CABI (2022)
Benin Present, no details CABI (2022)
Burkina Faso Present, no details CABI (2022)
Cameroon Present, no details Nicole et al. (1985), CABI (2022)
Central African Republic Present, no details CABI (2022)
Chad Present, no details CABI (1969)
Democratic Republic of the Present, no details CABI (2022)
Congo
Gabon Present, no details CABI (2022)
Ghana Present, no details CABI (2022)
Guinea Present, no details CABI (1969)
Ivory Cost Present, no details CABI (2022)
Kenya Present, no details CABI (2022)
Liberia Present, no details Nicole et al. (1985)
Mali Present, no details CABI (1969)
Mauritania Present, no details CABI (1969)
Nigeria Cross-River, Ondo, Present, no details CABI (2022)
Ikom
Senegal Present, no details CABI (1969)
Sierra Leone Present, no details CABI (2022)
Tanzania Present, no details CABI (2022)
Togo Present, no details CABI (2022)
Uganda Present, no details CABI (2022)
Asia China Present, no details Zhou et al. (2018)
Hong Kong Present, no details Stewart et al. (2020)
India Present, no details CABI (2022)
Indonesia Java, Sumatra Present, no details CABI (2022)
Japan Present, no details Akiba et al. (2015)
Malaysia Present, no details Stewart et al. (2020)
Myanmar Present, no details CABI (2022)
Pakistan Present, no details CABI (2022)
Philippines Present, no details Glen et al. (2014)
Singapore Present, no details CABI (2022)
Sri Lanka Present, no details Silva et al. (2017)
Taiwan Present, no details Hsiao et al. (2019), Ann et al. (2002)
Thailand Present, no details Samseemoung et al. (2011), Sunthudlakhar
et al. (2022)
Vietnam Present, no details CABI (2022)
(Continues)
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38 of 43 PYRRHODERMA NOXIUM: PEST CATEGORISATION
Sub-national (e.g.
Region Country state) Status References
Oceania American Samoa Present, no details Brooks (2002), Cannon et al. (2022)
Australia Present, no details Stewart et al. (2020)
Federated Stated of Chuuk, Kosrae, Present, no details Akiba et al. (2015), Cannon et al. (2022)
Micronesia Pohnpei, Yap
Fiji Present, no details CABI (2022)
French Polynesia Tahiti Present, no details Mallet et al. (1985)
Guam Present, no details Cannon et al. (2022)
Mariana Island Present, no details Cannon et al. (2022)
Niue Present, no details CABI (2022)
Papua New Guinea Present, no details CABI (2022)
Republic of Palau Present, no details Cannon et al. (2022)
Republic of Vanuatu Present, no details CABI (2022)
Rota Island Present, no details Cannon et al. (2022)
Saipan Present, no details Cannon et al. (2022)
Samoa Present, no details CABI (2022)
Solomon Islands Present, no details CABI (2022)
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PYRRHODERMA NOXIUM: PEST CATEGORISATION 39 of 43
APPE N D IX C
(Continues)
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PYRRHODERMA NOXIUM: PEST CATEGORISATION 41 of 43
(Continues)
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PYRRHODERMA NOXIUM: PEST CATEGORISATION 43 of 43
APPE N D IX D
Köppen–Geiger maps
Figure D.1 shows the Köppen–Geiger map for P. noxium based on report locations with geographical coordinates only.
Figure D.2 shows the Köppen–Geiger map for P. noxium based on report locations with and without geographical
coordinates.
F I G U R E D .1 Distribution of three Köppen–Geiger climate types, i.e. BSh, Cfa and Cfb, that occur in the EU and in third countries where
Pyrrhoderma noxium has been reported (locations with geographical coordinates only). The legend shows the list of Köppen–Geiger climates. Red
dots indicate point locations where P. noxium was reported.
F I G U R E D . 2 Koeppen–Geiger map based on the pathogen records with local geographical coordinates (as Figure 3), but also on those records
without local coordinates, which were thus assigned to large administrative areas (e.g. Pakistan, Japan), and thus include several climate types.