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. 2024 Mar 19;22(3):e8667. doi: 10.2903/j.efsa.2024.8667

Pest categorisation of Pyrrhoderma noxium

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
PMCID: PMC10949325  PMID: 38505477

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 saprophytically 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 environmental 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

1. INTRODUCTION

1.1. Background and Terms of Reference as provided by the requestor

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 commodities 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 derogations 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 imminent 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.

1.1.2. Terms of Reference

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 assessments 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 options 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.

1.2. Interpretation of the Terms of Reference

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 morphological 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.

1.3. Additional information

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 AND METHODOLOGIES

2.1. Data

2.1.1. Information on pest status from NPPOs

In the context of the current mandate, EFSA is preparing pest categorisations for new/emerging pests that are not yet regulated 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.

2.1.2. Literature search

A literature search on P. noxium was conducted at the beginning of the categorisation in the ISI Web of Science bibliographic database, using the scientific name of the pest as search term. Papers relevant for the pest categorisation were reviewed, 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.

2.1.3. Database search

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 notifications 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 categorisation 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.

TABLE 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 (Section 3.2 )

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.

Pest potential for entry, establishment and spread in the EU territory (Section 3.4 ) Is the pest able to enter into, become established in, and spread within, the EU territory? If yes, briefly list the pathways for entry and spread.
Potential for consequences in the EU territory (Section 3.5 ) Would the pests' introduction have an economic or environmental impact on the EU 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

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 determining 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, the Panel will seek to express potential EU impacts in terms of yield and quality losses and not in monetary terms, in agreement 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.

3. PEST CATEGORISATION

3.1. Identity and biology of the pest

3.1.1. Identity and taxonomy

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 consistent 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 noxium (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 species boundaries. The EPPO Global Database (EPPO, online) provides taxonomic identification only for the previous name Phellinus noxius, as followed:

Preferred name: Phellinus noxius (Corner) G. Cunningham

Order: Hymenochaetales

Family: Hymenochaetaceae

Genus: Phellinus

Species: Phellinus noxius

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 code 1 (EPPO, 2019; Griessinger & Roy, 2015) for this species is PHELNO (EPPO, online).

3.1.2. Biology of the pest

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 species 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, haemicellulose 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 generally 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 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.

3.1.3. Host range/species affected

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 encompasses 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.

3.1.4. Intraspecific diversity

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 geographically 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 hyphal 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 various 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).

3.1.5. Detection and identification of the pest

Are detection and identification methods available for the pest?

Yes, there are methods available for the detection and identification of Pyrrhoderma noxium.

Symptoms and signs

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, defoliation, 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 pathogens. 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 basidiocarps 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 absence 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 having 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).

FIGURE 1.

FIGURE 1

Global distribution of Pyrrhoderma noxium. Sources: systematic literature review (Section 2.1.2) and CABI (2022) (see Appendix B).

DNA‐based identification

The molecular techniques available for the identification of P. noxium are mostly based on the sequencing of the internal 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 evaluated 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 identify 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.

3.2. Pest distribution

3.2.1. Pest distribution outside the EU

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).

3.2.2. Pest distribution in the EU

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.

No. Pyrrhoderma noxium is not known to be present in the EU.

3.3. Regulatory status

3.3.1. Commission Implementing Regulation 2019/2072

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.

TABLE 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
Description CN code Third country, group of third countries or specific area of third country
1. Plants of […] Pinus L., […] other than fruit and seeds

ex 0602 20 20

ex 0602 20 80

ex 0602 90 41

ex 0602 90 45

ex 0602 90 46

ex 0602 90 47

ex 0602 90 50

ex 0602 90 70

ex 0602 90 99

ex 0604 20 20

ex 0604 20 40

Third countries other than: Albania, Andorra, Armenia, Azerbaijan, Belarus, Bosnia and Herzegovina, Canary Islands, Faeroe Islands, Georgia, Iceland, Liechtenstein, Moldova, Monaco, Montenegro, North Macedonia, Norway, Russia (only the following parts: Central Federal District (Tsentralny federalny okrug), Northwestern Federal District (Severo‐Zapadny federalny okrug), Southern Federal District (Yuzhny federalny okrug), North Caucasian Federal District (Severo‐Kavkazsky federalny okrug) and Volga Federal District (Privolzhsky federalny okrug)), San Marino, Serbia, Switzerland, Türkiye and Ukraine
2. Plants of […] and Quercus L., with leaves, other than fruit and seeds

ex 0602 10 90

ex 0602 20 20

ex 0602 20 80

ex 0602 90 41

ex 0602 90 45

ex 0602 90 46

ex 0602 90 48

ex 0602 90 50

ex 0602 90 70

ex 0602 90 99

ex 0604 20 90

ex 1404 90 00

Third countries other than: Albania, Andorra, Armenia, Azerbaijan, Belarus, Bosnia and Herzegovina, Canary Islands, Faeroe Islands, Georgia, Iceland, Liechtenstein, Moldova, Monaco, Montenegro, North Macedonia, Norway, Russia (only the following parts: Central Federal District (Tsentralny federalny okrug), Northwestern Federal District (Severo‐Zapadny federalny okrug), Southern Federal District (Yuzhny federalny okrug), North Caucasian Federal District (Severo‐Kavkazsky federalny okrug) and Volga Federal District (Privolzhsky federalny okrug)), San Marino, Serbia, Switzerland, Turkey and Ukraine
5.

Isolated bark of Quercus L., other

than Quercus suber L.

ex 1404 90 00

ex 4401 40 90

Canada, Mexico, United States
9. Plants for planting of […] Prunus L. and Pyrus L. and their hybrids […], other than seeds

ex 0602 10 90

ex 0602 20 20

ex 0602 90 30

ex 0602 90 41

ex 0602 90 45

ex 0602 90 46

ex 0602 90 48

ex 0602 90 50

ex 0602 90 70

ex 0602 90 91

ex 0602 90 99

Third countries other than Albania, Algeria, Andorra, Armenia, Australia, Azerbaijan, Belarus, Bosnia and Herzegovina, Canada, Canary Islands, Egypt, Faeroe Islands, Georgia, Iceland, Israel, Jordan, Lebanon, Libya, Liechtenstein, Moldova, Monaco, Montenegro, Morocco, New Zealand, North Macedonia, Norway, Russia (only the following parts: Central Federal District (Tsentralny federalny okrug), Northwestern Federal District (Severo‐ Zapadny federalny okrug), Southern Federal District (Yuzhny federalny okrug), North Caucasian Federal District (Severo‐ Kavkazsky federalny okrug) and Volga Federal District (Privolzhsky federalny okrug)), San Marino, Serbia, Switzerland, Syria, Tunisia, Turkey, Ukraine, the United Kingdom (1) and United States other than Hawaii
10. Plants of Vitis L., other than fruits

ex 0602 10 10

ex 0602 20 10

ex 0604 20 90

ex 1404 90 00

Third countries other than Switzerland
11. Plants of Citrus L., [………], and their hybrids, other than fruits and seeds

ex 0602 10 90

ex 0602 20 20

ex 0602 20 30

ex 0602 20 80

ex 0602 90 45

ex 0602 90 46

ex 0602 90 47

ex 0602 90 50

ex 0602 90 70

ex 0602 90 91

ex 0602 90 99

ex 0604 20 90

ex 1404 90 00

All third countries
20. Growing medium as such, other than soil, consisting in whole or in part of solid organic substances, other than that composed entirely of peat or fibre of Cocos nucifera L., previously not used for growing of plants or for any agricultural purposes

ex 2530 10 00

ex 2530 90 00

ex 2703 00 00

ex 3101 00 00

ex 3824 99 93

Third countries other than Switzerland

3.4. Entry, establishment and spread in the EU

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.

Comment on plants for planting as a pathway.

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:

  1. host plants for planting (excluding seeds for sowing),

  2. bark and wood (timber, logs, sawdust, wooden pallets) of host plants, and

  3. soil and other plant growing media associated with infected host plant debris, all originating in infested third countries.

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 considered 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.

TABLE 3.

Potential pathways for entry of Pyrrhoderma noxium into the EU.

Pathways (e.g. host/intended use/source) Life stage Relevant mitigations (e.g. prohibitions [Annex VI], special requirements [Annex VII] or phytosanitary certificates [Annex XI] within Implementing Regulation 2019/2072)
Host plants for planting, other than seeds Mycelium, basidiospores, arthrospores (if any) Several main hosts identified in Section 3.1.3 are included in Commission Implementing Regulation 2019/2072. There is a temporary prohibition for high‐risk plants (Regulation 2018/2019)
Parts of host plants, other than fruits and seeds (stems, roots) Mycelium, basidiospores, arthrospores (if any) A phytosanitary certificate is required for the introduction into the Union from third countries other than Switzerland, of parts of host plants other than fruits and seeds (Annex XI, Part B of Commission Implementing Regulation (EU) 2019/2072)
Soil as such not attached or associated with plants for planting Mycelium, basidiospores, arthrospores (if any) The introduction into the Union from third countries, other than Switzerland, of soil as such consisting in part of solid organic substances is banned (Annex VI (19) of Commission Implementing Regulation (EU) 2019/2072)
Growing medium as such, other than soil not attached or associated with plants for planting Mycelium, basidiospores, arthrospores (if any) A phytosanitary certificate is required for the introduction into the Union from third countries, other than Switzerland, of growing medium attached to or associated with plants, intended to sustain the vitality of the plants (Annex XI, Part A (1) of Commission Implementing Regulation (EU) 2019/2072). Special requirements also exist for this commodity (Annex VII (1) of Commission Implementing Regulation (EU) 2019/2072)
Growing medium, attached to or associated with host and non‐host plants for planting carrying infected plant debris, with the exception of sterile medium of in vitro plants Mycelium, basidiospores, arthrospores (if any) A phytosanitary certificate is required for the introduction into the Union from third countries, other than Switzerland, of growing medium attached to or associated with plants, intended to sustain the vitality of the plants (Annex XI, Part A (1) of Commission Implementing Regulation (EU) 2019/2072). Special requirements also exist for this commodity (Annex VII (1) of Commission Implementing Regulation (EU) 2019/2072)
Machinery and vehicles with contaminated soil and/or infected debris of host plants Mycelium, basidiospores, arthrospores (if any) A phytosanitary certificate is required for the introduction into the Union from third countries, other than Switzerland, of machinery and vehicles (Annex XI, Part A (1) of Commission Implementing Regulation (EU) 2019/2072). Special requirements also exist for this commodity (Annex VII (2) of Commission Implementing Regulation (EU) 2019/2072)

The quantity of fresh produce of main hosts imported into the EU from countries where P. noxium is present is provided in Table 4.

TABLE 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.

Commodity HS code 2016 2017 2018 2019 2020
Live forest trees 0602 90 56 98 243 138 88

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

Is the pest able to become established in the EU territory?

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 establishment 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.

3.4.2.1. EU distribution of main host plants

As noted above and shown in Appendix A, P. noxium has a wide host range, also considering that it is able to colonise several of those plant species endophytically or to survive as a saprophyte in dead plant debris. Some of its main hosts (e.g. Citrus spp., Prunus spp., Pyrus spp., including P. communis, Quercus sp., and Vitis vinifera; see Section 3.1.3) are widely distributed in the EU, both in commercial production (nurseries, open fields, orchards) and in home gardens, parks or forests. The harvested area of most of the main hosts of P. noxium cultivated in the EU in recent years is shown in Table 5.

TABLE 5.

Harvested area of some Pyrrhoderma noxium hosts relevant for the EU, 2017–2021 (1000 ha). Source: EUROSTAT (accessed November 2023).

Crop Code 2017 2018 2019 2020 2021
Grapes W1000 3133.32 3135.50 3155.20 3146.24 3120.22
Citrus fruits T0000 502.84 508.99 512.83 522.10 519.96
Peaches/nectarines F1210 F1220 221.64 214.97 206.87 203.32 194.01
Cherries F1240 173.37 175.49 176.30 178.61 175.71
Pears F1120 113.81 113.54 110.66 108.29 106.96
Apricots F1230 72.23 72.57 73.22 76.13 73.48
Avocados F2300 12.72 13.22 17.50 19.58 22.86
Bananas F2400 18.91 17.94 18.27 22.11 22.01
3.4.2.2. Climatic conditions affecting establishment

Based on the data available in the literature on the geographical coordinates of the locations from where P. noxium has been reported, the pathogen is present in non‐EU areas with BSh, Cfa and Cfb, Köppen–Geiger climate zones. These climate zones also occur in the EU, where hosts of P. noxium are grown (Appendix D). Appendix D also provides a Koeppen–Geiger map based on all P. noxium records, also those without local coordinates. For a more accurate description of geographical areas suitable for establishment, a hardiness zone map was generated. This map is based on the 30‐year average absolute minimum temperature and suggests that P. noxium would be able to establish in the EU, although in a restricted area along the Mediterranean (Figure 2). In addition, soil temperature maps (Figures 3 and 4) based on the temperature range (12–36°C) that allow P. noxium to grow (Ann, Lee, & Huang, 1999) also suggest that there are areas in the EU (coastal areas in Mediterranean countries) suitable for the establishment of this pathogen.

FIGURE 2.

FIGURE 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).

FIGURE 3.

FIGURE 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 days in seven classes. Data Source: Muñoz‐Sabater et al. (2021). Based on the 1993–2022 period.

FIGURE 4.

FIGURE 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.

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).

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 reported (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 contribute to the dispersal of basidiospores and arthrospores.

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 macrophyllus, Garcinia subelliptica, Delonix regia and Erythrina variegata (Abe et al., 1995). In the Ivory Coast, rubber tree (Hevea brasiliensis) 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.

3.6. Available measures and their limitations

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).

3.6.1. Identification of potential additional measures

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.

3.6.1.1. Additional potential risk reduction options

Potential additional control measures are listed in Table 6.

TABLE 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 (Blue underline = Zenodo doc, Blue = WIP) RRO summary Risk element targeted (entry/establishment/spread/impact)
Require pest freedom Plants, plant products and other objects must come from a pest‐free country or a pest‐free area or a pest‐free place of production Entry/Spread
Growing plants in isolation

Description of possible exclusion conditions that could be implemented to isolate the crop from pests and if applicable relevant vectors. E.g. a dedicated structure such as glass or plastic greenhouses

Growing nursery plants in isolation may represent an effective control measure

Entry/Establishment/Spread
Managed growing conditions Proper field drainage, plant distancing, use of pathogen‐free agricultural tools (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 Entry/Spread/Impact
Crop rotation, associations and density, weed/volunteer control

Crop rotation, associations and density, weed/volunteer control are used to prevent problems related to pests and are usually applied in various 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)

Establishment/Spread/Impact
Use of resistant and tolerant plant species/varieties
Resistant plants are used to restrict the growth and development of a specified pest and/or the damage they cause when compared to susceptible plant 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)

Entry/Establishment/Impact
Roguing and pruning

Roguing is defined as the removal of infested plants and/or uninfested host 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

Entry/Spread/Impact
Biological control, Biopesticides and behavioural manipulation

Biological control of P. noxium has been investigated at the laboratory scale only on leaf oils obtained from the plant Cinnamomum osmophloeum (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)

Entry/Impact
Chemical treatments on crops including reproductive material Various fungicides have been found to have activity against the pathogen (Lim et al., 1990; Mappes and Hiepko, 1984), but routine field treatments with these fungicides are not economical Entry/Establishment/Impact
Chemical treatments on consignments or during processing

Use of chemical compounds that may be applied to plants or to plant products after harvest, during process or packaging operations and storage

The treatments addressed in this information sheet are:
  1. fumigation;
  2. spraying/dipping pesticides;
  3. surface disinfectants;
  4. process additives;
  5. protective compounds

As an example, the treatment of pallets can be mentioned

Entry/Spread
Physical treatments on consignments or during processing

This information sheet deals with the following categories of physical treatments: irradiation/ionisation; mechanical cleaning (brushing, washing); 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

Entry/Spread
Cleaning and disinfection of facilities, tools and machinery

The physical and chemical cleaning and disinfection of facilities, tools, machinery, transport means, facilities and other accessories (e.g. boxes, 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

Entry/Spread
Limits on soil P. noxium survives in the soil and on plant debris in or on the soil surface. Therefore, plants, plant products and other objects (e.g. used farm machinery) should be free from soil to ensure freedom from P. noxium Entry/Spread
Soil treatment
The control of soil organisms by chemical and physical methods listed below:
  1. Fumigation;
  2. Heating;
  3. Solarisation;
  4. Flooding;
  5. Soil suppression;
  6. Augmentative Biological control;
  7. 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)

Entry/Establishment/Impact
Use of non‐contaminated water

Chemical and physical treatment of water to eliminate waterborne 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

Entry/Spread
Waste management
  • Treatment of the waste (deep burial, composting, incineration, chipping, 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

Establishment/Spread
Heat and cold treatments

Controlled temperature treatments aimed to kill or inactivate pests without 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

Entry/Spread
Conditions of transport
Specific requirements for mode and timing of transport of commodities to prevent escape of the pest and/or contamination.
  1. Physical protection of consignment
  2. 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.

Entry/Spread
Post‐entry quarantine and other restrictions of movement in the importing country

This information sheet covers post‐entry quarantine (PEQ) of relevant commodities; temporal, spatial and end‐use restrictions in the importing country for import of relevant commodities; Prohibition of import of 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

Establishment/Spread
3.6.1.2. Additional supporting measures

Potential additional supporting measures are listed in Table 7.

TABLE 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.

Supporting measure Summary Risk element targeted (entry/establishment/spread/impact)
Inspection and trapping Due to its possible endophytic lifestyle, P. noxium may remain quiescent or latent within asymptomatic host tissues. On symptomatic plants, the symptoms caused by P. noxium are similar to those caused by other root rot pathogens. Therefore, it is unlikely that P. noxium could be detected based on visual inspection only Entry/Establishment/Spread
Laboratory testing Macroscopic examination of the basidiocarps and of symptoms at the below ground parts of plants, microscopic examination of morphological features such mycelium, trichocysts and basidispores and DNA‐based identification allow the reliable detection and identification of P. noxium (see Section 3.1.5) Entry/Establishment/Spread
Sampling Necessary as part of other risk reduction options Entry/Establishment/Spread
Phytosanitary certificate and plant passport Recommended for plant species known to be hosts of P. noxium, including plant parts, but excluding seeds for sowing Entry/Spread
Certified and approved premises Certified and approved premises may reduce the likelihood of the plants and plant products originating in those premises to be infected by P. noxium Entry/Spread
Certification of reproductive material (voluntary/official) The risk of entry and/or spread of P. noxium is reduced if host plants for planting, excluding seeds for sowing, are produced under an approved certification scheme and tested free of the pathogen Entry/Spread
Delimitation of Buffer zones Delimitation of a buffer zone around an outbreak area can prevent spread of the pathogen and maintain a pest‐free area, site or place of production Spread
Surveillance Surveillance to guarantee that plants and plant products originate from a pest‐free area could be an option Entry/Establishment/Spread
3.6.1.3. Biological or technical factors limiting the effectiveness of measures
  • Latently infected (asymptomatic) host plants and plant products are unlikely to be detected by visual inspection.

  • The similarity of symptoms of P. noxium with those of other root rot pathogens poses a serious challenge to the detection and identification of the pathogen based solely on visual inspection of the above ground parts of hosts.

  • The wide host range of the pathogen and its ability to survive endophytically on asymptomatic plants limit the possibility to develop standard diagnostic protocols for all potential hosts.

3.7. Uncertainty

No key uncertainty was identified.

4. CONCLUSIONS

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).

TABLE 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).

Criterion of pest categorisation Panel's conclusions against criterion in regulation (EU) 2016/2031 regarding union quarantine pest Key uncertainties
Identity of the pest (Section 3.1 ) The identity of Pyrrhoderma noxium is clearly defined. The pathogen has been shown to produce consistent symptoms and to be transmissible None
Absence/presence of the pest in the EU (Section 3.2 ) Pyrrhoderma noxium is not known to be present in the EU None
Pest potential for entry, establishment and spread in the EU (Section 3.4 ) Pyrrhoderma noxium could potentially enter, established in and spread within the EU. The main pathways for entry of the pathogen into the EU are: (i) host plants for planting (ii) bark and wood of host plants and (iii) soil and other plant growing media containing plant debris, all originating in infested third countries. Both the biotic (host availability) and abiotic (climate suitability) factors occurring in parts of the EU where hosts are grown are favourable for the establishment of the pathogen. Following its establishment, the pathogen could spread within the EU by both natural and human‐assisted means None
Potential for consequences in the EU (Section 3.5 ) Pyrrhoderma noxium introduction into and spread within the EU may have an economic and environmental impact where hosts are grown None
Available measures (Section 3.6 ) Although not specifically targeted against P. noxium, existing phytosanitary measures mitigate the likelihood of the pathogen's entry, establishment and spread in the EU territory. Potential additional measures also exist to further mitigate the risk of introduction and spread of the pathogen in the EU None
Conclusion (Section 4 ) 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 None
Aspects of assessment to focus on/scenarios to address in future if appropriate: Further phylogenetic analyses would make it possible to better resolve P. noxium species boundaries

ABBREVIATIONS

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 distributed 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 prevents 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 contaminating 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 occupied spatial units.

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 introduction 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 present 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 phytosanitary 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).

CONFLICT 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.

COPYRIGHT FOR NON‐EFSA CONTENT

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.

PANEL MEMBERS

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.

APPENDIX A. Pyrrhoderma noxium host plants/species affected

A.1.

Host status Host name Plant family Common name Reference
Cultivated hosts Acacia auriculiformis Fabaceae Earleaf acacia Lewis and Arentz (1988)
Acacia confusa Fabaceae Taiwan acacia Ann et al. (2002), Akiba et al. (2015), Ann, Lee, and Tsai (1999), Hsiao et al. (2019)
Acacia crassicarpa Fabaceae Northern Wattle Ivory and Daruhi (1993)
Acacia excelsa Fabaceae Ironwood Cannon et al. (2022)
Acacia mangium Fabaceae Brown salwood Stewart et al. (2020)
Acacia nilotica Fabaceae Gum arabic tree Kutama et al. (2012)
Acaciella glauca (Syn. Leucaena glauca) Fabaceae Amourette, Redwood Heubel (1939)
Acer saccharum Aceraceae Sugar Maple Ibarra Caballero et al. (2020)
Actinodaphne pedicellata Lauraceae Litsea Ann et al. (2002)
Adenanthera pavonina Fabaceae Sandalwood Tree, red‐bead tree Brooks (2002), Cannon et al. (2022)
Agathis macrophylla Araucariaceae Fijian kauri Neil (1988)
Albizia falcataria (Syn. Falcataria falcata) Fabaceae Albizia Singh and Pandey (1989)
Albizia lebbeck Fabaceae Siris tree, Woman's Tongue, East Indian Walnut Hodges and Tenorio (1984)
Albizia spp. Fabaceae Ram (1975)
Aleurites fordii (Syn. Vernicia fordii) Euphorbiaceae Tung oil tree Ann et al. (2002)
Aleurites moluccanus Euphorbiaceae Candle nut tree Wu et al. (2011)
Aleurites montanus (Syn. Vernicia montana) Euphorbiaceae Wood oil tree Bertus (1935)
Alstonia scholaris Apocynaceae Blackboard tree Ann et al. (2002)
Amherstia nobilis Fabaceae Ann, Lee, and Tsai (1999)
Anacardium occidentale Anacardiaceae Cashew nut Supriadi et al. (2004)
Annona montana Annonaceae Mountain soursop Ann et al. (2002)
Annona squamosa Annonaceae Custard apple, Sugar apple Ann, Lee, and Huang (1999), Ann et al. (2002), Tsai et al. (2017)
Annona squamosa × A. cherimola Annonaceae Atimoya Ann et al. (2002)
Antiaris toxicaria Moraceae Bark cloth tree Neil (1988)
Antirhea chinensis Rubiaceae Bois goudron

Wu et al. (2011)

Aralia elata Araliaceae Angelica tree Sahashi et al. (2007)
Araucaria cunninghamii Araucariaceae Hoop pine Ann et al. (2002), Tsai et al. (2017), Hsiao et al. (2019)
Araucaria heterophylla Araucariaceae Norfolk Island pine Chang and Yang (1998), Ann et al. (2002)
Araucaria hunsteinii Araucariaceae Klinki Pine Singh and Pandey (1989)
Ardisia sieboldii Primulaceae Akiba et al. (2015), Sahashi et al. (2015)
Areca catechu Arecaceae Areca‐nut palm Farr et al. (2021)
Areca triandra Arecaceae Singh (1966)
Argusia argentea Boraginaceae Velvet soldierbush Sahashi et al. (2012)
Artocarpus Moraceae Riggenbach (1958)
Artocarpus altilis Moraceae Breadfruit Hsiao et al. (2019)
Artocarpus heterophyllus Moraceae Jack fruit Ann et al. (2002)
Averrhoa carambola Oxalidaceae Carambola, Star fruit Ann, Lee, and Huang (1999), Ann et al. (2002), Wu et al. (2011), Tsai et al. (2017)
Azadirachta excelsa Meliaceae Sentang Stewart et al. (2020)
Barringtonia asiatica Lecythidaceae Sea poison tree Brooks (2002), Cannon et al. (2022)
Barringtonia petiolata Lecythidaceae Ivory and Daruhi (1993)
Barringtonia samoensis Lecythidaceae Brooks (2002), Cannon et al. (2022)
Bauhinia × blakeana Fabaceae Hsiao et al. (2019), Stewart et al. (2020)
Bauhinia × hybrid Fabaceae Butterfly tree Ann et al. (2002), Tsai et al. (2017)
Bauhinia acuminata Fabaceae Dwarf white orchid tree Farr et al. (2021)
Bauhinia purpurea Fabaceae Purple bauhinia Ann et al. (2002)
Bauhinia racemosa Fabaceae Abe et al. (1995)
Bauhinia sp. Fabaceae Ann, Lee, and Tsai (1999)
Bauhinia variegata Fabaceae Orchid tree Ann et al. (2002), Tsai et al. (2017), Hsiao et al. (2019)
Betula papyrifera Betulaceae Paper birch Nicole et al. (1995)
Bidens pilosa Asteraceae Beggartick Chen et al. (2023)
Bischofia javanica Phyllanthaceae Autumn maple tree Ann et al. (2002), Sahashi et al. (2010, 2015)
Boehmeria nivea Urticaceae Ramio, China‐grass McIntosh (1951)
Bomba × ceiba Malvaceae Silk cotton Ann et al. (2002)
Bridelia monoica Phyllanthaceae Pop gun seed Wu et al. (2011)
Broussonetia kazinoki Moraceae Small paper mulberry Ann et al. (2002)
Broussonetia papyrifera Moraceae Paper mulberry Ann et al. (2002)
Burckella thurstonii Sapotaceae Singh et al. (1980)
Buxus bodinieri Buxaceae Sahashi et al. (2012)
Caesalpinia ferrea Fabaceae Brazilian ironwood Stewart et al. (2020)
Caesalpinia gilliesii Fabaceae Bird‐of‐paradise shrub Adra et al. (2022)
Cajanus cajan Fabaceae Bengal pea Stewart et al. (2020)
Callicarpa japonica Lamiaceae Japanese beautyberry Sahashi et al. (2012)
Calocedrus formosana Cupressaceae Taiwan incense cedar Ann et al. (2002), Tsai et al. (2017), Hsiao et al. (2019)
Calophyllum inophyllum Calophyllaceae Indian poon beauty leaf Abe et al. (1995), Ann et al. (2002), Akiba et al. (2015), Sahashi et al. (2010, 2015)
Calophyllum neoebudicum Calophyllaceae Brooks (2002), Cannon et al. (2022)
Camellia japonica Theaceae Camellia Ann et al. (2002)
Camellia sinensis Theaceae Tea Ann et al. (2002)
Cananga odorata Annonaceae Ylang‐ylang Brooks (2002), Cannon et al. (2022)
Canarium harveyi Burseraceae Brooks (2002), Cannon et al. (2022)
Carica papaya Caricaceae Papaya Neil (1988)
Cassia fistula Fabaceae Yellow golden shower tree Ann et al. (2002), Hsiao et al. (2019)
Cassia grandis Fabaceae Horse cassia Farr et al. (2021)
Cassia siamea Fabaceae Cassia tree Hsiao et al. (2019)
Casuarina equisetifolia Casuarinaceae Ironwood tree Abe et al. (1995), Ann et al. (2002), Sahashi et al. (2010, 2015), Wu et al. (2011), Akiba et al. (2015), Tsai et al. (2017)
Casuarina spp. Casuarinaceae Hodges and Tenorio (1984)
Casuarina torulosa Casuarinaceae Australian mahogany Farr et al. (2021)
Cedrela odorata Meliaceae Bastard cedar Farr et al. (2021)
Cedrela spp. Meliaceae Mallet et al. (1985)
Ceiba pentandra Malvaceae Kapok Ann et al. (2002), Stewart et al. (2020)
Ceiba speciosa Malvaceae Chorisia Akiba et al. (2015)
Celtis boninensis Cannabaceae Akiba et al. (2015), Sahashi et al. (2015)
Celtis sinensis Cannabaceae Chinese elm Tsang et al. (2020)
Celtis sp. Cannabaceae Steyaert (1948)
Cerbera manghas Apocynaceae Odollam cerberus tree Ann et al. (2002), Cannon et al. (2022)
Chamaecyparis formosensis Cupressaceae Taiwan red cypress Ann et al. (2002)
Chamaecyparis obtusa Cupressaceae Japanese false cypress Sahashi et al. (2014)
Chionanthus retusus Oleaceae Chinese fringe tree Chen et al. (2023)
Chorisia speciosa Malvaceae Floss silk tree Ann et al. (2002), Hsiao et al. (2019)
Chrysalidocarpus lutescens Arecaceae Yellow areca palm Ann et al. (2002), Hsiao et al. (2019)
Cinchona spp. Rubiaceae Riggenbach (1958)
Cinnamomum burmannii Lauraceae Cinnamon

Wu et al. (2011),

Stewart et al. (2020)

Cinnamomum camphora Lauraceae Camphor Ann et al. (2002), Tsai et al. (2017), Hsiao et al. (2019), Tsang et al. (2020)
Cinnamomum cassia Lauraceae Padang cassia Chung et al. (2015)
Cinnamomum doederleinii Lauraceae Akiba et al. (2015)
Cinnamomum insularimontanum Lauraceae Hsiao et al. (2019)
Cinnamomum japonicum Lauraceae Japanese cinnamon Sahashi et al. (2010)
Cinnamomum kanehirae Lauraceae Stout camphor Ann et al. (2002), Chung et al. (2015), Hsiao et al. (2019)
Cinnamomum osmophloeum Lauraceae Taiwan cinnamon Tsai et al. (2017)
Cinnamomum pseudopedunculatum Lauraceae Akiba et al. (2015), Sahashi et al. (2015)
Cinnamomum yabunikkei Lauraceae Akiba et al. (2015)
Cinnamomum zeylanicum (Syn. Cinnamomum verum) Lauraceae Ceylon cinnamon Ann et al. (2002)
Cinnamomum kotoense Lauraceae Botel tobago cinnamon tree Tsai et al. (2017)
Citrus limon Rutaceae Lemon Tsai et al. (2017)
Citrus limonia Rutaceae Mandarin lime Stewart et al. (2020)
Citrus spp. Rutaceae Farr et al. (2021)
Cleyera japonica Pentaphylacaceae Japanese cleyera Chung et al. (2015)
Cocos nucifera Arecaceae Coconut Farr et al. (2021)
Codiaeum variegatum Euphorbiaceae Croton Ann et al. (2002)
Coffea arabica Rubiaceae Coffee Ann et al. (2002)
Coffea liberica Rubiaceae Mallamaire (1935)
Cola nitida Malvaceae Kola Adebayo (1975)
Cordia alliodora Boraginaceae Ecuador laurel Neil (1986)
Cordia aspera Cordiaceae Brooks (2002), Cannon et al. (2022)
Cordia dichotoma Boraginaceae Cordia Ann et al. (2002)
Corymbia citriodora (Syn. Eucalyptus citriodora) Myrtaceae Lemon gum Ann et al. (2002), Tsai et al. (2017)
Crossostylis biflora Rhizophoraceae Brooks (2002), Cannon et al. (2022)
Cryptocarya concinnai Lauraceae Konishi crytocarya Ann et al. (2002)
Cryptomeria japonica Cupressaceae Japanese cedar Sahashi et al. (2014)
Cyathea lunulata (Syn. Sphaeropteris lunulata) Cyatheaceae Singh et al. (1980)
Cyathocaly × sp. Annonaceae Singh et al. (1980)
Cycas taitungensis Cycadaceae Chang and Yang (1998), Ann, Lee, and Huang (1999)
Cycas taiwaniana Cycadaceae Taiwan cycas Chang and Yang (1998), Ann et al. (2002)
Dalbergia sissoo Fabaceae Sissoo tree Ann et al. (2002)
Delonix regia Fabaceae Flame tree Abe et al. (1995), Ann et al. (2002), Tsai et al. (2017)
Dillenia biflora Dilleniaceae

Singh et al. (1980)

Dimocarpus longan Sapindaceae Longan Ann et al. (2002), Tsai et al. (2017)
Diospyros decandra Ebenaceae Ann, Lee, and Tsai (1999)
Diospyros egbert‐walkeri (Syn. Diospyros ferrea, D. vera) Ebenaceae Sea ebony Akiba et al. (2015)
Diospyros ferrea var. buxifolia Ebenaceae Philippine ebony persimmon Ann et al. (2002)
Diospyros kaki Ebenaceae Persimmon Ann, Lee, and Huang (1999), Ann et al. (2002), Tsai et al. (2017)
Diospyros oldhamii Ebenaceae Oldham persimmon Ann et al. (2002)
Diospyros samoensis Ebenaceae Brooks (2002), Cannon et al. (2022)
Distylium gracile Hamamelidaceae Hsiao et al. (2019)
Distylium lepidotum Hamamelidaceae Akiba et al. (2015), Shashi et al. (2015)
Distylium racemosum Hamamelidaceae Isu tree Akiba et al. (2015)
Dracaena draco Asparagaceae Dragon tree Stewart et al. (2020)
Dracaena fragrans Asparagaceae Dracena

Stewart et al. (2020)

Dracontomelon vitiense Anacardiaceae

Neil (1988)

Duranta repens (Syn. D. erecta) Verbenaceae Creeping sky flower Ann et al. (2002), Tsai et al. (2017)
Dypsis lutescens Arecaceae Yellow butterfly palm Huang et al. (2015)
Dysoxylum amooroides Meliaceae

Ivory and Daruhi (1993)

Dysoxylum richii Meliaceae

Singh et al. (1980)

Dysoxylum samoense Meliaceae Brooks (2002), Cannon et al. (2022)
Ehretia dichotoma Ehretiaceae

Sahashi et al. (2012)

Ehretia philippinensis Ehretiaceae Akiba et al. (2015)
Elaeagnus rotundata Elaeagnaceae Sahashi et al. (2015)
Elaeis guineensis Arecaceae African oil palm Pinruan et al. (2010)
Elaeis sp. Arecaceae Riggenbach (1958)
Elaeocarpus decipiens (Syn. Elaeocarpus zollingeri) Elaeocarpaceae Japanese blueberry tree Akiba et al. (2015)
Elaeocarpus kambi Elaeocarpaceae

Singh et al. (1980)

Elaeocarpus serratus Elaeocarpaceae Ceylon olive Ann et al. (2002)
Elaeocarpus sylvestris Elaeocarpaceae Chung et al. (2015)
Elateriospermum tapos Euphorbiaceae Tapos

Stewart et al. (2020)

Elattostachys falcata Sapindaceae Brooks (2002), Cannon et al. (2022)
Endospermum macrophyllum Euphorbiaceae

Singh et al. (1980)

Eriobotrya japonica Rosaceae Loquat Ann, Lee, and Huang (1999), Ann et al. (2002), Tsai et al. (2017)
Eriodendron Malvaceae Riggenbach (1958)
Erythrina Fabaceae Hodges and Tenorio (1984)
Erythrina lithosperma (Syn. Erythrina subumbrans) Fabaceae Ram (1975)
Erythrina variegata (Syn. E. indica) Fabaceae Indian coral tree Abe et al. (1995), Akiba et al. (2015), Shashi et al. (2015)
Erythrospermum acuminatissimum Achariaceae

Singh et al. (1980)

Eucalyptus camaldulensis Myrtaceae Murray red gum eucalyptus Ann et al. (2002)
Eucalyptus deglupta Myrtaceae

Ivory and Daruhi (1993)

Eucalyptus grandis Myrtaceae Maiden eucalyptus Ann et al. (2002)
Eucalyptus pellita Myrtaceae red mahogany Agustini et al. (2014), Glen et al. (2014)
Eucalyptus robusta Myrtaceae Beakpod eucalyptus Hsiao et al. (2019)
Eucalyptus spp. Myrtaceae

Sahashi et al. (2012),

Agustini et al. (2014), Farr et al. (2021)

Eucalyptus urophylla Myrtaceae Ivory and Daruhi (1993)
Eugenia uniflora Myrtaceae Surinam cherry, pitanga Akiba et al. (2015)
Euonymus boninensis Celastraceae

Sahashi et al. (2015)

Euphorbia pulcherrima Euphorbiaceae Ann, Tsai, Wang, and Hsien (1999)
Ficus benghalensis Moraceae Banyan

Akiba et al. (2015), Sahashi et al. (2015)

Ficus benjamina Moraceae Weeping fig Hsiao et al. (2019)
Ficus carica Moraceae Common fig Cannon et al. (2022)
Ficus drupacea Moraceae Chen et al. (2023)
Ficus elastica Moraceae Rubber plant Ann et al. (2002); Akiba et al. (2015), Sahashi et al. (2015), Hsiao et al. (2019)
Ficus hanceana (Syn. Ficus pumila) Moraceae Creeping fig Chang and Yang (1998)
Ficus macrocarpa Moraceae Small‐leafed banyan Ann et al. (2002)
Ficus macrophylla Moraceae Moreton Bay fig Gray (2017)
Ficus microcarpa Moraceae Curtain fig Akiba et al. (2015), Tsai et al. (2017), Tsang et al. (2020)
Ficus obliqua Moraceae Small‐leaved fig Brooks (2002), Cannon et al. (2022)
Ficus pumila var. awkeotsang (Syn. Ficus awkeotsang) Moraceae Jellyfig Ann, Lee, and Huang (1999), Ann et al. (2002), Tsai et al. (2017)
Ficus punctata Moraceae Ann, Lee, and Tsai (1999)
Ficus religiosa Moraceae Bo tree fig Ann et al. (2002), Tsai et al. (2017), Hsiao et al. (2019)
Ficus septica Moraceae

Neil (1988)

Ficus simplicissima Moraceae Asian fig Wu et al. (2011)
Ficus sp. Moraceae Brooks (2002), Cannon et al. (2022)
Ficus superba Moraceae Deciduous fig Chung et al. (2015)
Ficus tinctoria Moraceae Dye fig Brooks (2002), Akiba et al. (2015), Cannon et al. (2022)
Ficus variegata Moraceae Red‐stem fig Wu et al. (2011)
Ficus virgata Moraceae Akiba et al. (2015)
Firmiana simplex Sterculiaceae Chinese parasol Ann et al. (2002)
Flindersia brayleyana Rutaceae Singh and Pandey (1989)
Flemingia macrophylla Fabaceae Wild hop Farr et al. (2021)
Flueggea flexuosa Phyllanthaceae Brooks (2002), Cannon et al. (2022)
Fraxinus formosana Oleaceae Formosan ash Ann et al. (2002), Hsiao et al. (2019)
Garcinia mangostana Clusiaceae Mangosteen CABI (2022)
Garcinia myrtifolia Clusiaceae

Singh et al. (1980)

Garcinia subelliptica Clusiaceae Happiness tree, Fukugi tree Abe et al. (1995), Sahashi et al. (2010), Akiba et al. (2015)
Gardenia jasminoides Rubiaceae Cape jasmine Ann et al. (2002)
Garuga floribunda Burseraceae

Neil (1988)

Gleditsia fera Fabaceae

Stewart et al. (2020)

Gliricidia sepium Fabaceae Quick stick

Neil (1988)

Glochidion obovatum Euphorbiaceae Akiba et al. (2015)
Glochidion ramiflorum Phyllanthaceae Brooks (2002), Cannon et al. (2022)
Gmelina arborea Lamiaceae Snapdragon tree Brooks (2002)
Grevillea Proteaceae Riggenbach (1958)
Grevillea robusta Proteaceae Silver oak

Ann et al. (2002), Stewart et al. (2020)

Guamia mariannae (Syn. Meiogyne cylindrocarpa) Annonaceae

Stewart et al. (2020)

Heliotropium foertherianum Heliotropiaceae Tree heliotrope, Argusia Akiba et al. (2015)
Heritiera littoralis Malvaceae Looking glass tree Chen et al. (2023)
Heritiera sp. Malvaceae

Singh et al. (1980)

Hernandia nymphaeifolia Hernandiaceae Sea hearse Brooks (2002), Cannon et al. (2022)
Hevea brasiliensis Euphorbiaceae Rubber tree Brooks (2002)
Hevea sp. Euphorbiaceae Riggenbach (1958)
Hibiscus glaber Malvaceae Dwarf Mahoe Sahashi et al. (2015)
Hibiscus rosa‐sinensis Malvaceae Hibiscus Abe et al. (1995), Ann et al. (2002), Akiba et al. (2015)
Hibiscus schizopetalus Malvaceae Fringed hibiscus Ann et al. (2002)
Hibiscus tiliaceus Malvaceae Linden hibiscus Ann et al. (2002), Akiba et al. (2015), Cannon et al. (2022)
Hydrangea chinensis Hydrangeaceae Chinese hydrangea Ann et al. (2002)
Ilex mertensii Aquifoliaceae Sahashi et al. (2015)
Ilex rotunda Aquifoliaceae Round‐leaf holly Sahashi et al. (2007)
Inocarpus fagifer Fabaceae Brooks (2002), Cannon et al. (2022)
Intsia bijuga Fabaceae Moluccan ironwood Brooks (2002), Cannon et al. (2022)
Ixora chinensis Rubiaceae Jungle flame Chung et al. (2015)
Ixora x williamsii Hybrid Chung et al. (2015)
Jacaranda sp. Bignoniaceae Jacaranda Adra et al. (2022)
Jatropha integerrima (Syn. J. pandurifolia) Euphorbiaceae Peregrina Shashi et al. (2015)
Juniperus chinensis var. kaizuka Cupressaceae Dragon juniper Tsai et al. (2017)
Keteleeria davidiana var. formosana Pinaceae Taiwan keteleeria Ann et al. (2002)
Khaya ivorensis Meliaceae Singh and Pandey (1989)
Khaya senegalensis Meliaceae African mahogany Burcham et al. (2015), Wang et al. (2016)
Kigelia pinnata (Syn. Kigelia africana) Bignoniaceae Sausage tree Ann et al. (2002), Tsai et al. (2017)
Kleinhovia hospita Malvaceae Farr et al. (2021)
Koelreuteria elegans Sapindaceae Flamegold tree

Stewart et al. (2020)

Koelreuteria elegans var. formosana (Syn. Koelreuteria henryi) Sapindaceae Flame gold rain tree Ann et al. (2002), Tsai et al. (2017), Hsiao et al. (2019)
Koelreuteria paniculata Sapindaceae Golden rain tree CABI (2022)
Lagerstroemia micrantha Lythraceae Chung et al. (2015)
Lagerstroemia speciosa Lythraceae Queen's crepe myrtle Ann et al. (2002)
Lagerstroemia subcostata Lythraceae Sahashi et al. (2007)
Lagerstroemia turbinate Lythraceae Crepe myrtle Ann et al. (2002)
Lannea coromandelica Anacardiaceae Supriadi et al. (2004)
Lantana camara Verbenaceae Lantana Ann et al. (2002)
Larix kaempferi Pinaceae Sahashi et al. (2014)
Leptopetalum grayi Rubiaceae Sahashi et al. (2015)
Leucaena leucocephala Fabaceae White popinac Ann et al. (2002); Akiba et al. (2015), Sahashi et al. (2015)
Leucaena sp. Fabaceae Cannon et al. (2022)
Ligustrum japonicum Oleaceae Japanese privet

Sahashi et al. (2012)

Ligustrum micranthum Oleaceae Akiba et al. (2015), Shashi et al. (2015)
Liquidambar formosana Hamamelidaceae Formosa sweet gum Ann et al. (2002), Tsai et al. (2017), Hsiao et al. (2019)
Litchi chinensis Sapindaceae Litchi Ann, Lee, and Huang (1999); Ann et al. (2002); Akiba et al. (2015), Tsai et al. (2017)
Litsea glutinosa Lauraceae Indian laurel Ann et al. (2002)
Litsea hypophaea Lauraceae Mountain pepper Ann et al. (2002)
Litsea japonica Lauraceae Litsea Akiba et al. (2015)
Litsea monopetala Lauraceae Many flowered litsea

Wu et al. (2011)

Livistona chinensis Arecaceae Chinese fan palm

Wu et al. (2011)

Lophostemon confertus Myrtaceae Zhang et al. (2022)
Macaranga graeffeana Euphorbiaceae

Singh et al. (1980)

Macaranga harveyana Euphorbiaceae Brooks (2002), Cannon et al. (2022)
Macaranga mappa Euphorbiaceae Cannon et al. (2022)
Macaranga sp. Euphorbiaceae Liao et al. (2023)
Macaranga stipulosa Euphorbiaceae Brooks (2002), Cannon et al. (2022)
Macaranga tanarius Euphorbiaceae Macaranga Ann et al. (2002), Hsiao et al. (2019)
Macaranga tanarius var. tomentosa Euphorbiaceae Akiba et al. (2015)
Macaranga thompsonii Euphorbiaceae Pengua tree

Stewart et al. (2020)

Machilus chekiangensis Lauraceae

Zhang et al. (2022)

Machilus kobu Lauraceae Sahashi et al. (2015)
Machilus thunbergii (Syn. Persea thunbergii) Lauraceae Japanese bay tree, red machilus, tabunoki Sahashi et al. (2007, 2010), Akiba et al. (2015)
Machilus zuihoensis (Syn. Persea zuihoensis) Lauraceae Incense machilus Ann et al. (2002)
Maesa tenera Myrsinaceae Taiwan maesa Ann et al. (2002)
Mallotus paniculatus Euphorbiaceae Turn in the wind Ann et al. (2002), Tsang et al. (2020)
Malpighia emarginata Malpighiaceae Acerola Sahashi et al. (2015)
Mangifera indica Anacardiaceae Mango Akiba et al. (2015), Sahashi et al. (2015, 2017), Hsiao et al. (2019)
Maytenus diversifolia Celastraceae

Sahashi et al. (2012)

Melaleuca bracteata Myrtaceae Black tea tree Tsai et al. (2017)
Melaleuca leucadendron Myrtaceae Weeping paperbark Ann et al. (2002)
Melia azedarach Meliaceae China berry Ann et al. (2002), Akiba et al. (2015), Hsiao et al. (2019)
Melia azedarach var. subtripinnata Meliaceae Sahashi et al. (2010, 2015)
Melodinus angustifolius Apocynaceae Narrow leafed melodinus Ann et al. (2002)
Metroxylon sp. Arecaceae

Neil (1988)

Michelia compressa Magnoliaceae Formosan michelia Ann et al. (2002)
Michelia figo Magnoliaceae Banana magnolia Ann et al. (2002)
Michelia sp. Magnoliaceae Ann, Lee, and Tsai (1999)
Microcos paniculata Malvaceae Garden mint

Wu et al. (2011)

Morinda citrifolia Rubiaceae Indian mulberry Brooks (2002), Cannon et al. (2022)
Morus australis Moraceae Korean mulberry Akiba et al. (2015), Sahashi et al. (2015)
Muntingia calabura Muntingiaceae Indian cherry Ann et al. (2002)
Murraya paniculata Rutaceae Orange jasmine Ann et al. (2002), Tsai et al. (2017), Hsiao et al. (2019)
Musa acuminata x Musa balbisiana Musaceae Banana

Stewart et al. (2020)

Musa spp. Musaceae

Ivory and Daruhi (1993)

Musa textilis Musaceae Berwick (1949)
Myristica castaneifolia Myristicaceae

Singh et al. (1980)

Myristica fatua (Syn. Virola surinamensis) Myristicaceae Banak Brooks (2002), Cannon et al. (2022)
Nageia nagi Podocarpaceae Nagi Chung et al. (2015)
Nandina domestica Berberidaceae Orange jessamine Akiba et al. (2015)
Neolitsea parvigemma Lauraceae Small bud neolitsea Ann et al. (2002)
Neolitsea sericea Lauraceae Sahashi et al. (2015)
Neonauclea forsteri Rubiaceae Brooks (2002), Cannon et al. (2022)
Nerium oleander Apocynaceae Oleander Ann et al. (2002)
Ochroma lagopus Malvaceae Balsa tree Farr et al. (2021)
Ochrosia mariannensis Apocynaceae Fago

Stewart et al. (2020)

Ochrosia nakaiana Apocynaceae Sahashi et al. (2015)
Oncidium Gower Ramsey Orchidaceae Tsai et al. (2017)
Osmanthus fragrans Oleaceae Sweet Osmanthus Ann et al. (2002), Tsai et al. (2017)
Osmanthus insularis Oleaceae Akiba et al. (2015), Sahashi et al. (2015)
Osmoxylon sp. Araliaceae

Neil (1988)

Pachira macrocarpa (Syn. P. aquatica) Malvaceae Malabar chestnut Ann et al. (2002); Sahashi et al. (2015), Hsiao et al. (2019)
Palaquium formosanum Sapotaceae Formosan nato tree Ann et al. (2002)
Palaquium hornei Sapotaceae Singh et al. (1980)
Pandanus boninensis Pandanaceae Sahashi et al. (2015)
Pangium edule Achariaceae Ivory and Daruhi (1993)
Parinari insularum Chrysobalanaceae Singh et al. (1980)
Parinari laurina (Syn. Atuna excelsa subsp. racemosa) Chrysobalanaceae Atuna Singh et al. (1980)
Passiflora edulis Passifloraceae Purple Passion Fruit Ann, Tsai, Wang, and Hsien (1999)
Persea americana Lauraceae Avocado Ann et al. (2002), Stewart et al. (2020)
Persea kobu (Syn. Machilus kobu) Lauraceae Sahashi et al. (2015)
Phyllanthus myrtifolius Phyllanthaceae Ceylon mirtle Leung et al. (2020)
Pinus caribaea Pinaceae Almonicar (1992)
Pinus elliottii Pinaceae Farr et al. (2021)
Pinus luchuensis Pinaceae Luchu pine Abe et al. (1995)
Pinus ponderosa Pinaceae Ponderosa pine Ibarra Caballero et al. (2020)
Pinus spp. Pinaceae Ibarra Caballero et al. (2020)
Pinus thunbergii (syn. Pinus thunbergiana) Pinaceae Black pine Ann et al. (2002)
Piper nigrum Pinaceae Black Pepper Farr et al. (2021)
Pipturus argenteus Urticaceae

Brooks (2002),

Cannon et al. (2022)

Pistacia chinensis Anacardiaceae Chinese pistache Ann et al. (2002)
Pittosporum tobira Pittosporaceae Japanese pittosporum Akiba et al. (2015)
Planchonella grayana Sapotaceae

Brooks (2002),

Cannon et al. (2022)

Planchonella obovata Sapotaceae Sea gutta Akiba et al. (2015), Sahashi et al. (2015)
Planchonella samoensis Sapotaceae

Brooks (2002),

Cannon et al. (2022)

Planchonella torricellensis Sapotaceae Brooks (2002)
Podocarpus macrophyllus Podocarpaceae Yew Abe et al. (1995), Ann et al. (2002), Sahashi et al. (2010), Tsai et al. (2017)
Pometia pinnata Sapindaceae Brooks (2002), Cannon et al. (2022)
Pongamia pinnata Fabaceae Pongamia Ann et al. (2002)
Populus deltoides Salicaceae Poplar Singh and Pandey (1989)
Prunus armeniaca Rosaceae Apricot Tsai et al. (2017)
Prunus campanulata Rosaceae Taiwan cherry Tsai et al. (2017)
Prunus cerasoides var. campanulata (Syn. Cerasus campanulata) Rosaceae Bell‐flowered cherry Akiba et al. (2015), Sahashi et al. (2015)
Prunus mahaleb Rosaceae Mahaleb cherry Ibarra Caballero et al. (2020)
Prunus mume Rosaceae Japanese apricot, plum Ann et al. (2002), Tsai et al. (2017)
Prunus persica (syn. Amygdalus persica) Rosaceae Peach Ann et al. (2002), Tsai et al. (2017), Akiba et al. (2015)
Prunus serrulata Rosaceae Oriental cherry Chung et al. (2015)
Prunus spp. Rosaceae Ibarra Caballero et al. (2020)
Psidium cattleianum f. lucidum Myrtaceae Strawberry guava Sahashi et al. (2015)
Psidium guajava Myrtaceae Guava Tsai et al. (2017)
Pterocarpus indicus Fabaceae Rose wood Ann et al. (2002), Tsai et al. (2017)
Pterospermum acerifolium Malvaceae Chen et al. (2023)
Pyrus communis Rosaceae European pear Ann, Lee, and Huang (1999)
Pyrus pyrifolia Rosaceae Pear Ann, Lee, and Huang (1999), Ann et al. (2002), Tsai et al. (2017)
Pyrus sp. Rosaceae Chung et al. (2015)
Quercus sp. Fagaceae Chung et al. (2015)
Reevesia formosana Malvaceae Taiwan Reevesia Fu and Cheung (2023)
Rhaphiolepis indica var. umbellata Rosaceae India hawthorne Akiba et al. (2015), Sahashi et al. (2015)
Rhaphiolepis umbellata (Syn. Laurus umbellate) Rosaceae Japanese‐hawthorn Sahashi et al. (2010)
Rhododendron obtusum Ericaceae Rhododendron Ann et al. (2002)
Rhododendron simsii Ericaceae Sims's azalea Chung et al. (2015)
Rhus succedanea (Syn. Toxicodendron succedaneum) Anacardiaceae Japanese wax tree Sahashi et al. (2015)
Rhus taitensis Anacardiaceae Brooks (2002), Cannon et al. (2022)
Roystonea regia Arecaceae Royal palm Ann et al. (2002)
Salix babylonica Salicaceae Willow Ann et al. (2002)
Salix nigra Salicaceae Black willow Ibarra Caballero et al. (2020)
Salix spp. Salicaceae Ibarra Caballero et al. (2020)
Samanea saman Fabaceae Rain tree Brooks (2002), Cannon et al. (2022)
Santalum album Santalaceae Burgess et al. (2018)
Schefflera octophylla Araliaceae Scheffera Ann et al. (2002)
Schima mertensiana (Syn. Schima boninensis) Theaceae Akiba et al. (2015), Sahashi et al. (2015)
Schinus terebinthifolia Anacardiaceae Brazilian peppertree Tsai et al. (2017)
Scolopia saeva Salicaceae Stewart et al. (2020)
Sonneratia sp. Lythraceae Stewart et al. (2020)
Spathodea campanulata Bignoniaceae African tulip tree Tsai et al. (2017), Hsiao et al. (2019)
Spondias dulcis Anacardiaceae Otaheite apple Sahashi et al. (2015), Cannon et al. (2022)
Stachytarpheta jamaicensis Verbenaceae Jamaica vervain Sahashi et al. (2015)
Sterculia foetida Sterculiaceae Hazel sterculia Ann et al. (2002)
Sterculia lanceolata Malvaceae

Wu et al. (2011),

Huang et al. (2016)

Sterculia nobilis Malvaceae Ping pong Ann et al. (2002), Tsai et al. (2017)
Swietenia macrophylla Meliaceae Big leaved mahogany Hsiao et al. (2019)
Swietenia mahagoni Meliaceae Mahogany Ann et al. (2002)
Syzygium inophylloides Myrtaceae Brooks (2002), Cannon et al. (2022)
Syzygium samarangense Myrtaceae Wax apple Ann, Lee, and Huang (1999), Ann et al. (2002), Tsai et al. (2017)
Syzygium sp. Myrtaceae Brooks (2002), Cannon et al. (2022)
Tabebuia chrysantha Bignoniaceae Yellow golden bell tree Ann et al. (2002)
Taiwania cryptomerioides Chrysomelidae Taiwania Ann et al. (2002)
Tamarindus indica Fabaceae Tamarind tree Hsiao et al. (2019)
Taxodium distichum Cupressaceae Deciduous cypress Chung et al. (2015)
Tectona grandis Lamiaceae Teak Hsiao et al. (2019), Stewart et al. (2020)
Tephrosia vogelii Fabaceae Beeley (1938)
Terminalia boivinii Combretaceae Bovinii Ann et al. (2002)
Terminalia calamansanai Combretaceae Neil (1988)
Terminalia catappa Combretaceae Indian almond Ann et al. (2002); Akiba et al. (2015), Sahashi et al. (2015), Tsai et al. (2017)
Terminalia ivorensis Combretaceae Ivory Coast almond Cannon et al. (2022)
Terminalia richii Combretaceae Brooks (2002), Cannon et al. (2022)
Theobroma Malvaceae Riggenbach (1958)
Theobroma cacao Malvaceae Cocoa Brooks (2002)
Thevetia peruviana (Syn. Cascabela thevetia) Apocynaceae Lucky‐nut, Milk tree Ann, Tsai, Wang, and Hsien (1999)
Toona australis Meliaceae Neil (1988)
Toona sinensis (Syn. Cedrela sinensis) Meliaceae Chinese cedar Tsai et al. (2017)
Tournefortia argentea Boraginaceae Tree heliotrope Hsiao et al. (2019)
Trachelospermum asiaticum Apocynaceae Asiatic jasmine Sahashi et al. (2015)
Trema orientalis Ulmaceae Charcoal tree Akiba et al. (2015), Sahashi et al. (2015), Hsiao et al. (2019)
Ulmus parvifolia Ulmaceae Chinese elm Ann et al. (2002)
Veitchia spp. Arecaceae Neil (1988)
Vitis sp. Vitaceae Chung et al. (2015)
Vitis vinifera Vitaceae Grape Ann, Lee, and Huang (1999), Ann et al. (2002), Tsai et al. (2017)
Wikstroemia pseudoretusa Thymelaeaceae Sahashi et al. (2015)
Zanthoxylum ailanthoides var. boninshimae Rutaceae Japanese prickly ash Sahashi et al. (2015)
Zelkova formosana Ulmaceae Chung et al. (2015)
Zelkova serrata Ulmaceae Zelkova Ann et al. (2002), Hsiao et al. (2019)
Zelkova sp. Ulmaceae Ann, Lee, and Tsai (1999)
Ziziphus mauritiana Rhamnaceae Indian jujube Tsai et al. (2017)
Wild weed hosts Artemisia capillaris Asteraceae Wormwood Ann et al. (2002)
Artemisia princeps Asteraceae Mugwort Ann et al. (2002)
Dendrocnide sp. Urticaceae Neil (1988)
Digitaria ciliaris Poaceae Chen et al. (2023)
Ipomoea pes‐caprae Convolvulaceae Morning glory Ann et al. (2002)
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. Saurauia tristyla) Actinidiaceae Ann et al. (2002)
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/experimental host Calophyllum vexans Calophyllaceae Abe et al. (1995)
Cassia bicapsularis (Syn. Senna bicapsularis) Fabaceae Christmas bush Ann, Tsai, Wang, and Hsien (1999)
Citrus grandis (Syn. Citrus maxima) Rutaceae Pampelmuse Ann, Tsai, Wang, and Hsien (1999)
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. Dimocarpus longan) Sapindaceae Longan Ann, Lee, and Huang (1999)
Fagus crenata Fagaceae Siebold's beech, Japanese beech Abe et al. (1995)
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)

APPENDIX B. Distribution of Pyrrhoderma noxium

B.1.

Region Country Sub‐national (e.g. 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 Congo Present, no details CABI (2022)
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, Ikom Present, no details CABI (2022)
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)
Oceania American Samoa Present, no details Brooks (2002), Cannon et al. (2022)
Australia Present, no details Stewart et al. (2020)
Federated Stated of Micronesia Chuuk, Kosrae, Pohnpei, Yap Present, no details Akiba et al. (2015), Cannon et al. (2022)
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)

APPENDIX C. Harvested area of Pyrrhoderma noxium main hosts in the EU MS

C.1.

Harvested area of Pyrrhoderma noxium main hosts in the EU MS, 2017–2021 (1000 ha). Source: EUROSTAT (accessed November 2023).

Crop 2017 2018 2019 2020 2021
Grapes (W1000) 3133.32 3135.50 3155.20 3146.24 3120.22
Belgium 0.24 0.30 0.38 0.49 0.56
Bulgaria 34.11 34.11 30.05 28.74 28.53
Czechia 15.81 15.94 16.08 16.14 16.36
Denmark 0.00 0.00 0.00 0.00 0.00
Germany : : : : :
Estonia 0.00 0.00 0.00 0.00 0.00
Ireland 0.00 0.00 0.00 0.00 0.00
Greece 101.75 100.34 101.85 104.21 89.84
Spain 937.76 939.92 936.89 931.63 929.39
France 750.46 750.62 755.47 759.59 757.83
Croatia 21.90 20.51 19.82 21.45 21.21
Italy 670.09 675.82 697.91 703.90 702.67
Cyprus 5.93 6.67 6.67 6.18 6.16
Latvia 0.00 0.00 0.00 0.00 0.00
Lithuania 0.00 0.00 0.00 0.00 0.00
Luxembourg 1.26 1.25 1.24 1.24 1.23
Hungary 67.08 66.06 64.92 59.63 59.07
Malta 0.68 0.42 0.42 0.45 0.46
Netherlands 0.16 0.17 0.16 0.17 0.19
Austria 46.33 46.50 46.36 46.16 42.84
Poland 0.67 0.73 0.74 1.00 1.00
Portugal 178.95 179.25 175.65 175.67 175.62
Romania 175.32 172.80 176.34 165.60 163.61
Slovenia 15.86 15.65 15.57 15.29 14.90
Slovakia 8.47 8.01 7.92 7.73 7.75
Finland 0.00 0.00 0.00 0.00 0.00
Sweden 0.04 0.05 0.05 0.08 0.09
Citrus fruits (T0000) 2017 2018 2019 2020 2021
EU 502.84 508.99 512.83 522.10 519.96
Greece 43.47 46.26 44.23 45.62 41.16
Spain 294.26 297.62 296.48 297.97 300.50
France 4.27 4.39 4.61 6.80 6.77
Croatia 2.06 1.97 2.20 2.10 2.14
Italy 135.36 134.64 140.74 145.10 144.70
Cyprus 2.92 3.05 3.20 3.03 2.91
Malta 0.00 0.00 0.00 0.00 0.11
Portugal 20.51 21.07 21.37 21.48 21.68
Peaches (F1210) & nectarines (F1220) 2017 2018 2019 2020 2021
EU 221.64 214.97 206.87 203.32 194.01
Belgium 0.00 0.00 0.00 0.00 0.00
Bulgaria 3.89 3.52 3.21 2.78 2.67
Czechia 0.37 0.38 0.34 0.34 0.32
Denmark 0.00 0.00 0.00 0.00 0.00
Germany 0.00 0.00 0.00 0.00 0.00
Estonia 0.00 0.00 0.00 0.00 0.00
Ireland 0.00 0.00 0.00 0.00 0.00
Greece 41.38 42.65 41.41 45.43 38.55
Spain 84.22 80.31 77.69 72.13 72.06
France 9.32 9.10 9.03 11.66 11.77
Croatia 0.96 0.86 0.88 0.78 0.80
Italy 67.02 64.30 60.44 58.68 56.54
Cyprus 0.30 0.29 0.31 0.34 0.35
Latvia 0.00 0.00 0.00 0.00 0.00
Lithuania 0.00 0.00 0.00 0.00 0.00
Luxembourg 0.00 0.00 0.00 0.00 0.00
Hungary 5.62 5.20 5.06 4.17 4.14
Malta 0.00 0.00 0.00 0.00 0.00
Netherlands 0.00 0.00 0.00 0.00 0.00
Austria 0.16 0.18 0.18 0.18 0.18
Poland 2.13 2.12 2.15 0.80 1.00
Portugal 3.90 3.74 3.78 3.80 3.76
Romania 1.77 1.70 1.79 1.69 1.37
Slovenia 0.28 0.26 0.25 0.25 0.24
Slovakia 0.32 0.36 0.35 0.31 0.28
Finland 0.00 0.00 0.00 0.00 0.00
Sweden 0.00 0.00 0.00 0.00 0.00
Crop 2017 2018 2019 2020 2021
Cherries (F1240) 173.37 175.49 176.30 178.61 175.71
Belgium 1.40 1.14 1.14 1.12 1.13
Bulgaria 10.06 11.23 12.16 11.73 11.93
Czechia 2.11 2.07 2.16 2.15 2.12
Denmark 0.66 0.56 0.53 0.61 0.56
Germany 7.96 7.94 7.94 7.89 7.81
Estonia 0.01 0.00 0.00 0.01 0.00
Ireland 0.00 0.00 0.00 0.00 0.00
Greece 15.83 16.21 16.24 20.70 16.93
Spain 27.59 27.50 27.60 27.91 29.61
France 8.01 8.13 8.03 7.51 7.50
Croatia 3.53 2.94 2.85 3.12 3.20
Italy 29.27 29.16 29.21 29.01 28.06
Cyprus 0.23 0.22 0.23 0.23 0.22
Latvia 0.10 0.10 0.12 0.10 0.10
Lithuania 0.73 0.76 0.77 0.77 0.76
Luxembourg 0.00 0.00 0.00 0.00 0.00
Hungary 15.65 15.88 15.93 16.62 16.79
Malta 0.00 0.00 0.00 0.00 0.00
Netherlands 0.81 0.79 0.78 0.79 0.77
Austria 0.25 0.30 0.30 0.30 0.29
Poland 36.44 36.91 37.29 35.20 35.00
Portugal 6.30 6.14 6.50 6.49 6.41
Romania 6.02 7.06 6.09 5.94 6.12
Slovenia 0.19 0.20 0.21 0.22 0.22
Slovakia 0.19 0.21 0.20 0.16 0.13
Finland 0.00 0.00 0.00 0.00 0.00
Sweden 0.03 0.03 0.03 0.04 0.05
Pears (F1120) 2017 2018 2019 2020 2021
EU 113.81 113.54 110.66 108.29 106.96
Belgium 10.02 10.15 10.37 10.66 10.45
Bulgaria 0.45 0.57 0.70 0.50 0.55
Czechia 0.71 0.75 0.80 0.83 0.80
Denmark 0.30 0.29 0.30 0.30 0.30
Germany 2.14 2.14 2.14 2.14 2.14
Estonia 0.00 0.00 0.00 0.00 0.00
Ireland 0.00 0.00 0.00 0.00 0.00
Greece 4.07 4.41 4.34 5.42 4.37
Spain 21.89 21.33 20.62 20.22 20.02
France 5.25 5.24 5.25 5.90 5.89
Croatia 0.71 0.80 0.86 0.73 0.75
Italy 31.73 31.34 28.71 26.60 26.79
Cyprus 0.07 0.06 0.06 0.07 0.08
Latvia 0.20 0.20 0.20 0.20 0.20
Lithuania 0.82 0.82 0.82 0.85 0.85
Luxembourg 0.02 0.02 0.02 0.01 0.01
Hungary 2.90 2.84 2.81 2.62 2.74
Malta 0.00 0.00 0.00 0.00 0.00
Netherlands 9.70 10.00 10.09 10.00 10.07
Austria 0.46 0.49 0.50 0.54 0.55
Poland 7.26 7.30 7.22 5.80 5.60
Portugal 11.54 11.21 11.33 11.33 11.16
Romania 3.12 3.10 3.08 3.09 3.17
Slovenia 0.20 0.21 0.21 0.22 0.23
Slovakia 0.11 0.12 0.11 0.10 0.09
Finland 0.04 0.05 0.04 0.05 0.05
Sweden 0.12 0.11 0.10 0.11 0.11
Apricots (F1230) 2017 2018 2019 2020 2021
EU 72.23 72.57 73.22 76.13 73.48
Belgium 0.00 0.00 0.00 0.00 0.00
Bulgaria 2.90 2.55 2.91 1.84 3.06
Czechia 1.10 1.15 1.15 1.17 1.12
Denmark 0.00 0.00 0.00 0.00 0.00
Germany 0.23 0.23 0.23 0.23 0.23
Estonia 0.00 0.00 0.00 0.00 0.00
Ireland 0.00 0.00 0.00 0.00 0.00
Greece 7.31 7.94 8.35 12.24 8.96
Spain 21.00 20.57 20.24 19.78 19.44
France 12.20 12.27 12.28 12.08 11.88
Croatia 0.28 0.27 0.26 0.29 0.31
Italy 17.36 17.81 17.91 17.81 17.74
Cyprus 0.19 0.18 0.18 0.20 0.21
Latvia 0.00 0.00 0.00 0.00 0.00
Lithuania 0.00 0.00 0.00 0.00 0.00
Luxembourg 0.00 0.00 0.00 0.00 0.00
Hungary 4.97 5.04 4.99 5.94 6.05
Malta 0.00 0.00 0.00 0.00 0.00
Netherlands 0.00 0.00 0.00 0.00 0.00
Austria 0.79 0.83 0.82 0.83 0.86
Poland 0.96 0.97 1.06 0.90 0.90
Portugal 0.56 0.56 0.54 0.52 0.53
Romania 2.11 1.97 2.04 2.03 1.92
Slovenia 0.08 0.08 0.08 0.09 0.09
Slovakia 0.19 0.16 0.18 0.20 0.19
Finland 0.00 0.00 0.00 0.00 0.00
Sweden 0.00 0.00 0.00 0.00 0.00
Crop 2017 2018 2019 2020 2021
Avocados (F2300) 12.72 13.22 17.50 19.58 22.86
Greece 0.60 0.72 1.08 1.10 1.93
Spain 11.81 12.16 14.10 15.85 18.06
France 0.23 0.24 0.24 0.13 0.13
Cyprus 0.08 0.10 0.10 0.16 0.17
Portugal 0.00 0.00 1.98 2.34 2.57
Crop 2017 2018 2019 2020 2021
Bananas (F2400) 18.91 17.94 18.27 22.11 22.01
Greece 0.09 0.09 0.10 0.10 0.10
Spain 9.08 9.09 9.06 9.10 9.10
France 8.49 7.50 7.78 11.58 11.48
Cyprus 0.21 0.22 0.21 0.22 0.21
Portugal 1.04 1.05 1.12 1.12 1.12

APPENDIX D. Köppen–Geiger maps

D.1.

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.

FIGURE D.1.

FIGURE 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.

FIGURE D.2.

FIGURE 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.

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. 10.2903/j.efsa.2024.8667

Adopted: 22 February 2024

Notes

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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