Pest categorisation of small‐spored Alternaria carrying the genes for the AM‐ or AK‐toxin biosynthesis

Abstract

The Panel on Plant Health performed a pest categorisation of small‐spored Alternaria carrying the genes for the AM‐ or AK‐toxin biosynthesis, for the EU. The identity of the pests is clearly defined and reliable methods exist for their detection/identification. They are listed in Annex IIAI of Directive 2000/29/EC as Alternaria alternata (non‐European pathogenic isolates). Their distribution in the EU is restricted though with some uncertainty. The AM‐toxin producer Alternaria affect Malus spp. and Pyrus communis (European pear), whereas the AK‐toxin producer affect Pyrus pyrifolia, Pyrus bretschneideri and Pyrus ussuriensis (Asian pears). The pests could potentially enter the EU on host‐planting material and fruit originating in infested countries. There are no biotic/abiotic factors limiting their potential establishment and spread in the EU, as their epidemiology is similar to that of other well‐established Alternaria spp. Apples and European pears are widespread in the EU; Japanese pears are also present, but no data was found on their abundance/distribution. In the infested areas, the pests cause premature defoliation, fruit spotting and rot resulting in yield/quality losses. It is expected that the introduction and spread of the pests in the EU could impact apple and pear production, although the magnitude is unknown. Cultural practices and chemical measures may reduce the inoculum and the disease, but they cannot eliminate the pests. Phytosanitary measures are available to mitigate the risk of introduction and spread of the pests. The pests do not meet all the criteria assessed by EFSA for consideration as potential Union quarantine pests, as they are not under official control in those EU restricted areas where they have been found. The pests do not meet all the criteria assessed by EFSA to consider them as Union regulated non‐quarantine pests, as host plants for planting are not the main means of pest spread.

1. Introduction

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

1.1.1. Background

Council Directive 2000/29/EC1 on protective measures against the introduction into the Community of organisms harmful to plants or plant products and against their spread within the Community establishes the present European Union plant health regime. The Directive lays down the phytosanitary provisions and the control checks to be carried out at the place of origin on plants and plant products destined for the Union or to be moved within the Union. In the Directive's 2000/29/EC annexes, the list of harmful organisms (pests) whose introduction into or spread within the Union is prohibited, is detailed together with specific requirements for import or internal movement.

Following the evaluation of the plant health regime, the new basic plant health law, Regulation (EU) 2016/20312 on protective measures against pests of plants, was adopted on 26 October 2016 and will apply from 14 December 2019 onwards, repealing Directive 2000/29/EC. In line with the principles of the above‐mentioned legislation and the follow‐up work of the secondary legislation for the listing of EU regulated pests, EFSA is requested to provide pest categorizations of the harmful organisms included in the annexes of Directive 2000/29/EC, in the cases where recent pest risk assessment/ pest categorisation is not available.

1.1.2. Terms of Reference

EFSA is requested, pursuant to Article 22(5.b) and Article 29(1) of Regulation (EC) No 178/20023, to provide scientific opinion in the field of plant health.

EFSA is requested to prepare and deliver a pest categorisation (step 1 analysis) for each of the regulated pests included in the appendices of the annex to this mandate. The methodology and template of pest categorisation have already been developed in past mandates for the organisms listed in Annex II Part A Section II of Directive 2000/29/EC. The same methodology and outcome is expected for this work as well.

The list of the harmful organisms included in the annex to this mandate comprises 133 harmful organisms or groups. A pest categorisation is expected for these 133 pests or groups and the delivery of the work would be stepwise at regular intervals through the year as detailed below. First priority covers the harmful organisms included in Appendix 1, comprising pests from Annex II Part A Section I and Annex II Part B of Directive 2000/29/EC. The delivery of all pest categorisations for the pests included in Appendix 1 is June 2018. The second priority is the pests included in Appendix 2, comprising the group of Cicadellidae (non‐EU) known to be vector of Pierce's disease (caused by Xylella fastidiosa), the group of Tephritidae (non‐EU), the group of potato viruses and virus‐like organisms, the group of viruses and virus‐like organisms of Cydonia Mill., Fragaria L., Malus Mill., Prunus L., Pyrus L., Ribes L., Rubus L. and Vitis L. and the group of Margarodes (non‐EU species). The delivery of all pest categorisations for the pests included in Appendix 2 is end 2019. The pests included in Appendix 3 cover pests of Annex I Part A Section I and all pest categorisations should be delivered by end 2020.

For the above‐mentioned groups, each covering a large number of pests, the pest categorisation will be performed for the group and not the individual harmful organisms listed under “such as” notation in the Annexes of the Directive 2000/29/EC. The criteria to be taken particularly under consideration for these cases, is the analysis of host pest combination, investigation of pathways, the damages occurring and the relevant impact.

Finally, as indicated in the text above, all references to ‘non‐European’ should be avoided and replaced by ‘non‐EU’ and refer to all territories with the exception of the Union territories as defined in Article 1 point 3 of Regulation (EU) 2016/2031.

1.1.2.1. Terms of Reference: Appendix 1

List of harmful organisms for which pest categorisation is requested. The list below follows the annexes of Directive 2000/29/EC.

Annex IIAI
(a) Insects, mites and nematodes, at all stages of their development
Aleurocantus spp.	Numonia pyrivorella (Matsumura)
Anthonomus bisignifer (Schenkling)	Oligonychus perditus Pritchard and Baker
Anthonomus signatus (Say)	Pissodes spp. (non‐EU)
Aschistonyx eppoi Inouye	Scirtothrips aurantii Faure
Carposina niponensis Walsingham	Scirtothrips citri (Moultex)
Enarmonia packardi (Zeller)	Scolytidae spp. (non‐EU)
Enarmonia prunivora Walsh	Scrobipalpopsis solanivora Povolny
Grapholita inopinata Heinrich	Tachypterellus quadrigibbus Say
Hishomonus phycitis	Toxoptera citricida Kirk.
Leucaspis japonica Ckll.	Unaspis citri Comstock
Listronotus bonariensis (Kuschel)
(b) Bacteria
Citrus variegated chlorosis	Xanthomonas campestris pv. oryzae (Ishiyama) Dye and pv. oryzicola (Fang. et al.) Dye
Erwinia stewartii (Smith) Dye
(c) Fungi
Alternaria alternata (Fr.) Keissler (non‐EU pathogenic isolates)	Elsinoe spp. Bitanc. and Jenk. Mendes
Anisogramma anomala (Peck) E. Müller	Fusarium oxysporum f. sp. albedinis (Kilian and Maire) Gordon
Apiosporina morbosa (Schwein.) v. Arx	Guignardia piricola (Nosa) Yamamoto
Ceratocystis virescens (Davidson) Moreau	Puccinia pittieriana Hennings
Cercoseptoria pini‐densiflorae (Hori and Nambu) Deighton	Stegophora ulmea (Schweinitz: Fries) Sydow & Sydow
Cercospora angolensis Carv. and Mendes	Venturia nashicola Tanaka and Yamamoto
(d) Virus and virus‐like organisms
Beet curly top virus (non‐EU isolates)	Little cherry pathogen (non‐ EU isolates)
Black raspberry latent virus	Naturally spreading psorosis
Blight and blight‐like	Palm lethal yellowing mycoplasm
Cadang‐Cadang viroid	Satsuma dwarf virus
Citrus tristeza virus (non‐EU isolates)	Tatter leaf virus
Leprosis	Witches’ broom (MLO)
Annex IIB
(a) Insect mites and nematodes, at all stages of their development
Anthonomus grandis (Boh.)	Ips cembrae Heer
Cephalcia lariciphila (Klug)	Ips duplicatus Sahlberg
Dendroctonus micans Kugelan	Ips sexdentatus Börner
Gilphinia hercyniae (Hartig)	Ips typographus Heer
Gonipterus scutellatus Gyll.	Sternochetus mangiferae Fabricius
Ips amitinus Eichhof
(b) Bacteria
Curtobacterium flaccumfaciens pv. flaccumfaciens (Hedges) Collins and Jones
(c) Fungi
Glomerella gossypii Edgerton	Hypoxylon mammatum (Wahl.) J. Miller
Gremmeniella abietina (Lag.) Morelet

1.1.2.2. Terms of Reference: Appendix 2

List of harmful organisms for which pest categorisation is requested per group. The list below follows the categorisation included in the annexes of Directive 2000/29/EC.

Annex IAI
(a) Insects, mites and nematodes, at all stages of their development
Group of Cicadellidae (non‐EU) known to be vector of Pierce's disease (caused by Xylella fastidiosa), such as:
1) Carneocephala fulgida Nottingham	3) Graphocephala atropunctata (Signoret)
2) Draeculacephala minerva Ball
Group of Tephritidae (non‐EU) such as:
1) Anastrepha fraterculus (Wiedemann)	12) Pardalaspis cyanescens Bezzi
2) Anastrepha ludens (Loew)	13) Pardalaspis quinaria Bezzi
3) Anastrepha obliqua Macquart	14) Pterandrus rosa (Karsch)
4) Anastrepha suspensa (Loew)	15) Rhacochlaena japonica Ito
5) Dacus ciliatus Loew	16) Rhagoletis completa Cresson
6) Dacus curcurbitae Coquillet	17) Rhagoletis fausta (Osten‐Sacken)
7) Dacus dorsalis Hendel	18) Rhagoletis indifferens Curran
8) Dacus tryoni (Froggatt)	19) Rhagoletis mendax Curran
9) Dacus tsuneonis Miyake	20) Rhagoletis pomonella Walsh
10) Dacus zonatus Saund.	21) Rhagoletis suavis (Loew)
11) Epochra canadensis (Loew)
(c) Viruses and virus‐like organisms
Group of potato viruses and virus‐like organisms such as:
1) Andean potato latent virus	4) Potato black ringspot virus
2) Andean potato mottle virus	5) Potato virus T
3) Arracacha virus B, oca strain	6) non‐EU isolates of potato viruses A, M, S, V, X and Y (including Yo, Yn and Yc) and Potato leafroll virus
Group of viruses and virus‐like organisms of Cydonia Mill., Fragaria L., Malus Mill., Prunus L., Pyrus L., Ribes L.,Rubus L. and Vitis L., such as:
1) Blueberry leaf mottle virus	8) Peach yellows mycoplasm
2) Cherry rasp leaf virus (American)	9) Plum line pattern virus (American)
3) Peach mosaic virus (American)	10) Raspberry leaf curl virus (American)
4) Peach phony rickettsia	11) Strawberry witches’ broom mycoplasma
5) Peach rosette mosaic virus	12) Non‐EU viruses and virus‐like organisms of Cydonia Mill., Fragaria L., Malus Mill., Prunus L., Pyrus L., Ribes L., Rubus L. and Vitis L.
6) Peach rosette mycoplasm
7) Peach X‐disease mycoplasm
Annex IIAI
(a) Insects, mites and nematodes, at all stages of their development
Group of Margarodes (non‐EU species) such as:
1) Margarodes vitis (Phillipi)	3) Margarodes prieskaensis Jakubski
2) Margarodes vredendalensis de Klerk

1.1.2.3. Terms of Reference: Appendix 3

List of harmful organisms for which pest categorisation is requested. The list below follows the annexes of Directive 2000/29/EC.

Annex IAI
(a) Insects, mites and nematodes, at all stages of their development
Acleris spp. (non‐EU)	Longidorus diadecturus Eveleigh and Allen
Amauromyza maculosa (Malloch)	Monochamus spp. (non‐EU)
Anomala orientalis Waterhouse	Myndus crudus Van Duzee
Arrhenodes minutus Drury	Nacobbus aberrans (Thorne) Thorne and Allen
Choristoneura spp. (non‐EU)	Naupactus leucoloma Boheman
Conotrachelus nenuphar (Herbst)	Premnotrypes spp. (non‐EU)
Dendrolimus sibiricus Tschetverikov	Pseudopityophthorus minutissimus (Zimmermann)
Diabrotica barberi Smith and Lawrence	Pseudopityophthorus pruinosus (Eichhoff)
Diabrotica undecimpunctata howardi Barber	Scaphoideus luteolus (Van Duzee)
Diabrotica undecimpunctata undecimpunctata Mannerheim	Spodoptera eridania (Cramer)
Diabrotica virgifera zeae Krysan & Smith	Spodoptera frugiperda (Smith)
Diaphorina citri Kuway	Spodoptera litura (Fabricus)
Heliothis zea (Boddie)	Thrips palmi Karny
Hirschmanniella spp., other than Hirschmanniella gracilis (de Man) Luc and Goodey	Xiphinema americanum Cobb sensu lato (non‐EU populations)
Liriomyza sativae Blanchard	Xiphinema californicum Lamberti and Bleve‐Zacheo
(b) Fungi
Ceratocystis fagacearum (Bretz) Hunt	Mycosphaerella larici‐leptolepis Ito et al.
Chrysomyxa arctostaphyli Dietel	Mycosphaerella populorum G. E. Thompson
Cronartium spp. (non‐EU)	Phoma andina Turkensteen
Endocronartium spp. (non‐EU)	Phyllosticta solitaria Ell. and Ev.
Guignardia laricina (Saw.) Yamamoto and Ito	Septoria lycopersici Speg. var. malagutii Ciccarone and Boerema
Gymnosporangium spp. (non‐EU)	Thecaphora solani Barrus
Inonotus weirii (Murril) Kotlaba and Pouzar	Trechispora brinkmannii (Bresad.) Rogers
Melampsora farlowii (Arthur) Davis
(c) Viruses and virus‐like organisms
Tobacco ringspot virus	Pepper mild tigré virus
Tomato ringspot virus	Squash leaf curl virus
Bean golden mosaic virus	Euphorbia mosaic virus
Cowpea mild mottle virus	Florida tomato virus
Lettuce infectious yellows virus
(d) Parasitic plants
Arceuthobium spp. (non‐EU)
Annex IAII
(a) Insects, mites and nematodes, at all stages of their development
Meloidogyne fallax Karssen	Rhizoecus hibisci Kawai and Takagi
Popillia japonica Newman
(b) Bacteria
Clavibacter michiganensis (Smith) Davis et al. ssp. sepedonicus (Spieckermann and Kotthoff) Davis et al.	Ralstonia solanacearum (Smith) Yabuuchi et al.
(c) Fungi
Melampsora medusae Thümen	Synchytrium endobioticum (Schilbersky) Percival
Annex I B
(a) Insects, mites and nematodes, at all stages of their development
Leptinotarsa decemlineata Say	Liriomyza bryoniae (Kaltenbac
(b) Viruses and virus‐like organisms
Beet necrotic yellow vein virus

1.2. Interpretation of the Terms of Reference

Alternaria alternata (non‐European pathogenic isolates) is one of a number of pests listed in the Appendices to the Terms of Reference (ToR) to be subject to pest categorisation to determine whether it fulfils the criteria of a harmful regulated pest or those of a regulated non‐quarantine pest for the area of the European Union (EU) excluding Ceuta, Melilla and the outermost regions of Member States (MSs) referred to in Article 355(1) of the Treaty on the Functioning of the European Union (TFEU), other than Madeira and the Azores.

The EU legislation refers to non‐European isolates of A. alternata (Fr.) Keissler that are pathogenic to Cydonia Mill., Malus Mill. and Pyrus L.

Based on recent literature revising the taxonomic status and pathogenicity of A. alternata (Andrew et al., 2009; Rotondo et al., 2012; Harteveld et al., 2013; Woudenberg et al., 2015), this pest categorisation focuses on the small‐spored Alternaria carrying the genes for the biosynthesis of the host‐specific AM‐ or AK‐toxin, in short ‘AM‐/AK‐toxin producer Alternaria’ (see Section 3.1.1).

2. Data and methodologies

2.1. Data

2.1.1. Literature search

A search of literature (1997–2017) in the ISI Web of Science bibliographic database was conducted at the beginning of the categorisation. The search focussed on A. alternata and its geographic distribution, life cycle, host plants and the damage it causes. The following search terms (TS) and combinations were used: TS=(“Alternaria alternata” OR “Alternaria alternata f. sp. mali” or “Alternaria alternata f. sp. kikuchiana” OR “Alternaria leaf blotch” OR “black spot of pears”) AND TS=(geograph* OR distribution OR “life cycle” OR lifecycle OR host OR hosts OR plant* OR damag*).

Further references and information were obtained from experts, from citations within the references and grey literature.

2.1.2. Database search

Pest information, on host(s) and distribution, was retrieved from the EPPO Global Database (EPPO, 2017).

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.

The Europhyt database was consulted for pest‐specific notifications on interceptions and outbreaks. Europhyt is a web‐based network launched by the Directorate General for Health and Consumers (DG SANCO), and is a subproject of PHYSAN (Phyto‐Sanitary Controls) specifically concerned with plant health information. The Europhyt database manages 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 MSs and the phytosanitary measures taken to eradicate or avoid their spread.

2.2. Methodologies

The Panel performed the pest categorisation for the AM‐/AK‐toxin producer Alternaria, following guiding principles and steps presented in the EFSA guidance on the harmonised framework for pest risk assessment (EFSA PLH Panel, 2010) and as defined in the International Standard for Phytosanitary Measures No 11 (FAO, 2013) and No 21 (FAO, 2004).

In accordance with the guidance on a harmonised framework for pest risk assessment in the EU (EFSA PLH Panel, 2010), this work was initiated following an evaluation of the EU's plant health regime. Therefore, to facilitate the decision‐making process, in the conclusions of the pest categorisation, the Panel addresses explicitly each criterion for a Union quarantine pest and for a Union regulated non‐quarantine pest in accordance with Regulation (EU) 2016/2031 on protective measures against pests of plants and includes additional information required as per the specific ToR received by the European Commission. In addition, for each conclusion, the Panel provides a short description of its associated uncertainty.

Table 1 presents the Regulation (EU) 2016/2031 pest categorisation criteria on which the Panel bases its conclusions. All relevant criteria have to be met for the pest to potentially qualify either as a quarantine pest or as a regulated non‐quarantine pest. If one of the criteria is not met, the pest will not qualify. A pest that does not qualify as a quarantine pest may still qualify as a regulated non‐quarantine pest which needs to be addressed in the opinion. For the pests regulated in the protected zones only, the scope of the categorisation is the territory of the protected zone; thus, the criteria refer to the protected zone instead of the EU territory.

Table 1.

Pest categorisation criteria under evaluation, as 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	Criterion in Regulation (EU) 2016/2031 regarding Union quarantine pest	Criterion in Regulation (EU) 2016/2031 regarding protected zone quarantine pest (articles 32–35)	Criterion in Regulation (EU) 2016/2031 regarding Union regulated non‐quarantine pest
Identity of the pest (Section  3.1 )	Is the identity of the pest established, or has it been shown to produce consistent symptoms and to be transmissible?	Is the identity of the pest established, or has it been shown to produce consistent symptoms and to be transmissible?	Is the identity of the pest established, 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 widely distributed within the EU? Describe the pest distribution briefly!	Is the pest present in the EU territory? If not, it cannot be a protected zone quarantine organism.	Is the pest present in the EU territory? If not, it cannot be a regulated non‐quarantine pest. (A regulated non‐quarantine pest must be present in the risk assessment area).
Regulatory status (Section  3.3 )	If the pest is present in the EU but not widely distributed in the risk assessment area, it should be under official control or expected to be under official control in the near future.	The protected zone system aligns with the pest‐free area system under the International Plant Protection Convention (IPPC). The pest satisfies the IPPC definition of a quarantine pest that is not present in the risk assessment area (i.e. protected zone).	Is the pest regulated as a quarantine pest? If currently regulated as a quarantine pest, are there grounds to consider its status could be revoked?
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!	Is the pest able to enter into, become established in, and spread within, the protected zone areas? Is entry by natural spread from EU areas where the pest is present possible?	Is spread mainly via specific plants for planting, rather than via natural spread or via movement of plant products or other objects? Clearly state if plants for planting is the main pathway!
Potential for consequences in the EU territory (Section  3.5 )	Would the pests’ introduction have an economic or environmental impact on the EU territory?	Would the pests’ introduction have an economic or environmental impact on the protected zone areas?	Does the presence of the pest on plants for planting have an economic impact, as regards the intended use of those plants for planting?
Available measures (Section  3.6 )	Are there measures available to prevent the entry into, establishment within or spread of the pest within the EU such that the risk becomes mitigated?	Are there measures available to prevent the entry into, establishment within or spread of the pest within the protected zone areas such that the risk becomes mitigated? Is it possible to eradicate the pest in a restricted area within 24 months (or a period longer than 24 months where the biology of the organism so justifies) after the presence of the pest was confirmed in the protected zone?	Are there measures available to prevent pest presence on plants for planting such that the risk becomes mitigated?
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.	A statement as to whether (1) all criteria assessed by EFSA above for consideration as potential protected zone quarantine pest were met, and (2) if not, which one(s) were not met.	A statement as to whether (1) all criteria assessed by EFSA above for consideration as a potential regulated non‐quarantine pest were met, and (2) if not, which one(s) were not met.

It should be noted that 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, the Panel will present a summary of the observed pest impacts. Economic impacts are expressed in terms of yield and quality losses and not in monetary terms, while addressing social impacts is outside the remit of the Panel, in agreement with EFSA guidance on a harmonised framework for pest risk assessment (EFSA PLH Panel, 2010).

The Panel will not indicate in its conclusions of the pest categorisation whether to continue the risk assessment process, but, following the agreed two‐step approach, will continue only if requested by the risk managers. However, during the categorisation process, experts may identify key elements and knowledge gaps that could contribute significant uncertainty to a future assessment of risk. It would be useful to identify and highlight such gaps so that potential future requests can specifically target the major elements of uncertainty, perhaps suggesting specific scenarios to examine.

3. Pest categorisation

3.1. Identity and biology of the pest

3.1.1. Identity and taxonomy

Is the identity of the pest established, or has it been shown to produce consistent symptoms and to be transmissible?

Yes, the identity of the pests is well‐established

To clarify the identity of the pest considered in the EU legislation, the following background information and taxonomic notes are provided.

Alternaria alternata includes both saprophytic and pathogenic isolates. Pathogenicity is mainly related to toxin production. Some isolates produce host‐specific toxins (HSTs) and are pathogenic to specific hosts, including apple, as well as European and Japanese pears; genes for HST biosynthesis are located in a single locus in the genome on single small dispensable chromosomes (Tsuge et al., 2012). Other isolates produce non‐HSTs targeting basic cellular processes and causing cell damage (Meena et al., 2016) to several hosts of different genera.

The A. alternata pathogenic isolates, mentioned in the EU legislation, are those isolates carrying genes for HST biosynthesis. In the EPPO Global database and CABI Invasive Species Compendium, they are named Alternaria mali and Alternaria gaisen (syn. Alternaria kikuchiana) and they produce the AM and AK HSTs, causing Alternaria leaf blotch/fruit spot of apple and black spot of pear, respectively. In the literature, these isolates have also been considered either pathotypes (A. alternata apple pathotype, A. alternata Japanese pear pathotype) or formae speciales (A. alternata f. sp. mali and A. alternata f. sp. kikuchiana) of A. alternata (Nishimura, 1980; Woudenberg et al., 2015).

Species of Alternaria were traditionally defined based on spore characteristics and sporulation patterns (Simmons, 1992). Alternaria spp. that share colony and conidial morphological characteristics have been classified into several morphological species groups, for instance Alternaria tenuissima, Alternaria arborescens and A. alternata species groups (Simmons, 1992, 1994, 1995; Simmons and Roberts, 1993). These morphological species groups were later considered as phylogenetic groups in molecular and metabolite profiling studies (Pryor and Gilbertson, 2000; Andersen et al., 2001; Woudenberg et al., 2013, 2015). Phylogenetic studies have demonstrated a clear distinction between large‐ and small‐spored Alternaria species, but boundaries among the small‐spored taxa have been a subject of controversy (Andrew et al., 2009). Strains of the former A. alternata, including those producing the AM‐ or the AK‐toxin, are now reclassified in different small‐spored taxa (Rotondo et al., 2012; Harteveld et al., 2013).

There is no consensus yet between taxonomists regarding relationships between Alternaria species, and specifically A. alternata and the biosynthesis of HSTs (EFSA CONTAM Panel, 2011). Additionally, it has been suggested that horizontal chromosome transfer may occur between Alternaria isolates, conferring the ability for non‐pathogenic Alternaria isolates to produce a HST and, thus, become pathogenic on specific hosts (Tsuge et al., 2012).

Therefore, this pest categorisation focuses on small‐spored Alternaria carrying the AM‐ or AK‐toxin genes, which correspond to A. mali and A. gaisen, respectively, reported in the EPPO Global Database and CABI Invasive Species Compendium.

Based on the above, the pests considered in the EU legislation belong to the family Pleosporaceae, to the genus Alternaria, to different small‐spored species groups, and carry the genes for the AM‐ or AK‐toxin biosynthesis (in short, for this pest categorisation, ‘AM‐/AK‐toxin producer Alternaria’).

3.1.2. Biology of the pest

Studies from Japan and Korea indicate that the pest (as A. mali) overwinters as conidia on apple leaves, buds and twigs (Lee and Lee, 1972; Sekiguchi, 1976). Filajdić and Sutton (1995) studied the overwintering of A. mali in apple orchards in North Carolina, USA. Leaves on the ground were considered the most important source of overwintering conidia. Harteveld et al. (2014) also indicated that in Australia, overwintering of the pest occurred mainly in leaf residue and to a lesser extent on twigs and buds. Filajdić and Sutton (1995) indicated that relatively low inoculum levels are enough for disease development.

Lesions on overwintered leaves resume sporulation, inducing inoculum build‐up and initiating primary infections. Afterwards, environmental conditions in late spring determine epidemic development. The optimum temperature for infection, mycelial growth, sporulation and spore germination of small‐spored AM‐ and AK‐toxin producer Alternaria is 25–30°C and 24–28°C, respectively (Sakuma, 2014; Sawamura, 2014). Filajdić and Sutton (1992a) studied the relationship of temperature and leaf wetness duration on the severity of Alternaria blotch of apple in North Carolina, USA. They estimated an optimum temperature for infection of 23.5°C, with 5.1 hours of leaf wetness required for a low disease severity (i.e. 0.2% leaf area covered with lesions). Filajdić and Sutton (1992a) indicated an incubation period (from infection to symptom expression) of 1–2 days for A. mali. This short incubation period is a common feature of the HST producer Alternaria, and it was related to the rapid action of these toxins on their specific target plant tissues (Tsuge et al., 2012).

In Korea, Kim et al. (1986) indicated a temperature threshold and four subsequent rain events for the occurrence of Alternaria leaf blotch of apple. After disease onset, the progress of epidemics was related to the frequency of rains. Kim et al. (1986) also found a significant linear relationship between disease progress and cumulative number of airborne conidia of A. mali. Likewise, in Australia, the most significant period of spore production on the canopy coincided with the stage of fruit growth (Harteveld et al., 2014). In Australia, Alternaria leaf blotch infection began about 20 days after full bloom and the highest disease incidence occurred from 70 to 110 days after bloom. Fruit infection occurred about 100 days after bloom (Harteveld et al., 2014).

There is little information on the biology of the pest (as A. gaisen) on Pyrus pyrifolia. Tanaka (1933) indicated that the optimum conditions for infection were 24–30°C and relative humidity over 90%. Likewise, Hsieh and Chiu (1974) reported optimal mycelial growth at 23°C. These conditions are also favourable for most Alternaria species affecting different crops (Rotem, 1994).

3.1.3. Detection and identification of the pest

Are detection and identification methods available for the pest?

Yes, the AK‐/AM‐toxin producer Alternaria can be detected and identified based on host association, symptomatology and cultural/morphological characteristics of their colonies in agar media combined with molecular methods for the detection of the genes responsible for the AM‐ or the AK‐toxin biosynthesis.

The AM‐ and AK‐toxin producer Alternaria cause leaf blotch/fruit spot on apples and black spot on pears, respectively. Nevertheless, host association and symptomatology are not sufficient for the detection of the pests, as similar symptoms are caused by other biotic or abiotic agents. Moreover, morphological and cultural characteristics are not reliable for the identification of the pests, as other small‐spored Alternaria, not being AM‐ or AK‐toxin producers, have similar cultural and morphological characteristics. Reliable detection and identification of the pests are only possible by the application of molecular methods to detect the genes responsible for the AM‐ or AK‐toxin biosynthesis (Johnson et al., 2000; Roberts, 2005; Andersen et al., 2006).

Symptoms

Symptoms caused on apples

The first symptoms of the disease appear on leaves in late spring or late summer as small, round, brown to blackish spots, gradually enlarging to 2–5 mm in diameter, with a brownish purple border (Sawamura, 2014). Later, most of those lesions undergo secondary enlargement and become irregular and much darker acquiring a frogeye appearance. If the lesions appear on petioles, the leaves turn yellow and drop prematurely. Symptoms on the current year's shoots appear as round, blackish to brown spots, slightly sunken and bordered by cracks. Sometimes, lenticels appear swollen because of the infection. Only fruit of the susceptible cultivars develop small necrotic spots, which enlarge during the summer.

Symptoms caused on Asian pears

Leaves, petioles, shoots, fruit, flower buds, pistils and flower petals of Asian pears are affected by the disease (Sakuma, 2014). Symptoms on leaves appear as tiny, round, black spots, which enlarge to a diameter of about 10 mm. These large lesions show blackish brown centres. If a lesion appears on a vein, it develops along the midrib and forms in an irregular shape. Severely infected leaves fall prematurely. Lesions, larger than those on leaves, may appear on fruit at any stage of their development resulting in cracking and preharvest fruit drop. Shoot lesions are round, blackish to brown and become sunken and cracked around the margins as they age. Infected flower buds decay and do not sprout during the next flowering season.

Morphology

The several small‐spored AM‐toxin producer Alternaria reported worldwide to be associated with leaf blotch and fruit spot of apples do not have uniform morphological characteristics except for the small, concatenated, multicellular conidia (dictyoconidia) produced in acropetal chains on short conidiophores in bushy clumps (Rotem, 1994).

The conidiophores of the small‐spored AK‐toxin producer Alternaria are olive brown, fasciculate, simple or branched. The conidia (6–22 × 9.5–69.5 μm) are olive to olive brown, mostly oblong, ovate (rarely obclavate), muriform, packet‐shaped, with 1–10 transverse and 1–3 longitudinal septa. Conidia do not have a true beak (Sakuma, 2014).

3.2. Pest distribution

3.2.1. Pest distribution outside the EU

The EPPO Global Database provides the geographical distribution of the AM‐/AK‐toxin producer Alternaria as A. mali (Figure 1, Table 2) and A. gaisen (Figure 2, Table 3) reported worldwide on Malus spp. and P. pyrifolia showing leaf blotch/fruit spot and fruit black spot symptoms, respectively.

Figure 1.

Global distribution map for Alternaria mali extracted from the EPPO Global Database (last updated: 13/9/2017; last accessed: 22/11/2017). According to Gur et al. (2017), small‐spored Alternaria carrying the gene for AM‐toxin biosynthesis are present in Israel. The pests (as A. mali) are also present in Pakistan (CABI, 2017)

Table 2.

Global distribution of small‐spored AM‐toxin producer Alternaria based on information extracted from the EPPO Global Database (as A. mali) (last updated: 13/9/2017; last accessed: 11/10/2017), CABI Invasive Species Compendium (as A. mali) (last updated: 12/7/2017; last accessed: 11/10/2017) and other sources

Continent	Country	Status	Sources
America	Canada	Present, restricted distribution	EPPO
	Chile	Present, no details	EPPO
	United States of America	Present, restricted distribution	EPPO
Asia	China	Present, no details	EPPO
	India	Present, no details	EPPO
	Iran	Present, restricted distribution	EPPO
	Israel	Present	Gur et al. (2017)
	Japan	Present, widespread	EPPO
	Korea, Republic	Present, no details	EPPO
	Pakistan	Present	CABI
	Taiwan	Present, restricted distribution	EPPO
Europe	Serbia	Present, few occurrences	EPPO
	Turkey	Present, restricted distribution	EPPO
Oceania	Australia	Present, restricted distribution	EPPO

Figure 2.

Global distribution map for Alternaria gaisen extracted from the EPPO Global Database (last updated: 13/9/2017; last accessed: 27/9/2017). According to CABI Invasive Species Compendium (2017), A. gaisen is also present in Pakistan

Table 3.

Global distribution of small‐spored AK‐toxin producer Alternaria based on information extracted from the EPPO Global Database (as A. gaisen) (last updated: 30/9/2016; last accessed: 11/10/2017) and CABI Invasive Species Compendium (as A. gaisen) (last updated: 22/6/2017; last accessed: 22/11/2017)

Continent	Country	Status	Sources
Asia	China	Present, restricted distribution	EPPO
	Japan	Present, widespread	EPPO
	Korea, Republic	Present, no details	EPPO
	Pakistan	Present	CABI
	Taiwan	Present, restricted distribution	EPPO

There is uncertainty with respect to the distribution of the AM‐/AK‐toxin producer Alternaria on Malus spp. and Pyrus spp. outside the EU, particularly for those reports where identification was based on morphological observations and pathogenicity tests, and not on the detection of the genes responsible for the biosynthesis of the AM‐ or the AK‐toxin (see Section 1.2).

3.2.2. Pest distribution in the EU

Is the pest present in the EU territory?

Yes, small‐spored Alternaria carrying the gene for the AM‐ or AK‐toxin biosynthesis are known to be present in the EU territory.

If present, is the pest widely distributed within the EU?

The distribution of the pests in the risk assessment area may be considered restricted, with some uncertainty.

Small‐spored Alternaria carrying the gene for the AM‐toxin biosynthesis are present in Denmark and Italy (Table 4).

Table 4.

Current distribution of small‐spored AM‐toxin producer Alternaria in the 28 EU MS based on information from the EPPO Global Database (as A. mali) (last updated: 13/9/2017; last accessed: 11/10/2017) and other sources

Country	Status	Sources
Denmark	Presenta	Andersen et al. (2006)
Italy	Presenta	Rotondo et al. (2012)
Netherlands	Absent, confirmed by survey	EPPO

^aThe gene for the AM‐toxin biosynthesis was also detected.

In Denmark, two small‐spored Alternaria isolates originating from apple flowers and tested positive for the AM‐toxin gene were used in Andersen et al. (2006) phenotypic studies.

In northern Italy, symptoms similar to those described for Alternaria blotch (Tweedy and Powell, 1962) appeared in Alto Adige on apple leaves and fruits, starting from 1990s. Alternaria spp. were isolated from these lesions and one representative isolate was compared with a reference strain and identified as A. alternata. Pathogenicity tests carried out with that isolate and cultural filtrates showed typical Alternaria blotch symptoms (Marschall and Bertagnoll, 2006). Later, the disease was also observed in Trentino (Gobber et al., 2004) and the isolation and pathogenicity of A. alternata were confirmed. The disease has also been found in Lombardy (ERSAF, 2016), Friuli (ERSA, 2015), Veneto (Anonymous, 2017), Piedmont (Anonymous, 2015) even though pathogenicity tests were not performed.

Rotondo et al. (2012) carried out a further study by using a collection of 173 isolates from different areas in northern Italy and four reference strains, three of which were Japanese strains of small‐spored Alternaria pathogenic on apple and one was a type isolate for A. mali. Isolates have been characterised based on: (i) morphological characters, following Simmons (2002), to determine their ‘species group’; (ii) pathogenicity by using a bioassay on both leaves and fruit, based on artificial inoculation with spore suspensions and culture filtrates; (iii) molecular analysis to determine the presence of the AM‐toxin gene following Johnson et al. (2000). Of the 173 isolates, 44 were pathogenic and belonged to the following species groups: A. tenuissima, A. arborescens, and A. alternata; three of the four reference strains exhibited A. tenuissima sporulation habit, while one was characterised by an A. arborescens sporulation pattern. Ten of these pathogenic isolates were positive for the presence of the AM‐toxin gene, as the three Japanese strains did. Therefore, the production of the AM‐toxin may be involved in pathogenesis by some of the Italian isolates of Alternaria from apple.

According to the EPPO Global Database and CABI Invasive Species Compendium, small‐spored AK‐toxin producer Alternaria are present in France, Hungary and Italy (Table 5).

Table 5.

Current distribution of small‐spored AK‐toxin producer Alternaria in the 28 EU MS based on information from the EPPO Global Database (as A. gaisen) (last updated: 30/9/2016; last accessed: 11/10/2017), CABI Invasive Species Compendium (as A. gaisen) (last updated: 22/6/2017; last accessed: 11/10/2017), and other sources

Country	Status	Sources
France	Present, few occurrences	EPPO
Greece	Absent, invalid record	EPPO
Hungary	Present	CABI
Italy	Present, restricted distribution	EPPO
Netherlands	Absent, intercepted only	EPPO
Portugala	Present	Woudenberg et al. (2015)

^aHost plant unknown.

There is uncertainty with respect to the distribution of the AM‐/AK‐toxin producer Alternaria on Malus spp. and Pyrus spp. in the EU, particularly for those reports where identification was based on morphological observations and pathogenicity tests, and not on the detection of the genes responsible for the biosynthesis of the AM‐ or the AK‐toxins.

3.3. Regulatory status

3.3.1. Council Directive 2000/29/EC

Small‐spored AM‐/AK‐toxin producer Alternaria (as A. alternata) are listed in Council Directive 2000/29/EC. Details are presented in Tables 6 and 7.

Table 6.

Small‐spored AM‐/AK‐toxin producer Alternaria (as Alternaria alternata) in Council Directive 2000/29/EC

Annex II, Part A	Harmful organisms whose introduction into, and spread within, all member states shall be banned if they are present on certain plants or plant products
Section I	Harmful organisms not known to occur in the community and relevant for the entire community
(c)	Fungi
	Species	Subject of contamination
1.	Alternaria alternata (Fr.) Keissler (non‐European pathogenic isolates)	Plants of Cydonia Mill., Malus Mill. and Pyrus L. intended for planting, other than seeds, originating in non‐European countries

Table 7.

Regulated hosts and commodities that may involve small‐spored AM‐/AK‐toxin producer Alternaria (as Alternaria alternata) in Annexes III, IV and V of Council Directive 2000/29/EC

Annex III, Part A	Plants, plant products and other objects the introduction of which shall be prohibited in all Member States
	Description	Country of origin
9.	Plants of Chaenomeles Ldl., Cydonia Mill., Crateagus L., Malus Mill., Prunus L., Pyrus L., and Rosa L., intended for planting, other than dormant plants free from leaves, flowers and fruit	Non‐European countries
18.	Plants of Cydonia Mill., Malus Mill., Prunus L. and Pyrus L. and their hybrids, and Fragaria L., intended for planting, other than seeds	Without prejudice to the prohibitions applicable to the plants listed in Annex III A (9), where appropriate, non‐European countries, other than Mediterranean countries, Australia, New Zealand, Canada, the continental states of the USA
Annex V	Plants, plant products and other objects which must be subject to a plant health inspection (at the place of production if originating in the Community, before being moved within the Community — in the country of origin or the consignor country, if originating outside the Community) before being permitted to enter the Community
Part A	Plants, plant products and other objects originating in the Community
Section I	Plants, plant products and other objects which are potential carriers of harmful organisms of relevance for the entire Community and which must be accompanied by a plant passport
1.1	Plants, intended for planting, other than seeds, of Amelanchier Med., Chaenomeles Lindl., Cotoneaster Ehrh., Crataegus L., Cydonia Mill., Eriobotrya Lindl., Malus Mill., Mespilus L., Photinia davidiana (Dcne.) Cardot, Prunus L., other than Prunus laurocerasus L. and Prunus lusitanica L., Pyracantha Roem., Pyrus L. and Sorbus L.
Part B	Plants, plant products and other objects originating in territories, other than those referred to in Part A
Section I	Plants, plant products and other objects which are potential carriers of harmful organisms of relevance for the entire Community
3.	Fruits of: 1–  Citrus L., Fortunella Swingle, Poncirus Raf., and their hybrids, Momordica L. and Solanum melongena L., 2–  Annona L., Cydonia Mill., Diospyros L., Malus Mill., Mangifera L., Passiflora L., Prunus L., Psidium L., Pyrus L., Ribes L. Syzygium Gaertn., and Vaccinium L., originating in non‐European countries, 3–  Capsicum L.

3.3.2. Legislation addressing the hosts of small‐spored AM‐/AK‐toxin producer Alternaria (as Alternaria alternata)

Additional movement restrictions for the hosts exist in relation to other pests, such as Erwinia amylovora or Apple proliferation mycoplasma.

3.4. Entry, establishment and spread in the EU

3.4.1. Host range

The main hosts of small‐spored AM‐toxin producer Alternaria (as A. mali or A. alternata f. sp. mali or A. alternata apple pathotype) are Malus spp. and Pyrus communis (European pear) (Tanahashi et al., 2016; EPPO, 2017).

The small‐spored AK‐toxin producer Alternaria (as A. gaisen or A. kikuchiana or A. alternata f. sp. kikuchiana or A. alternata Japanese pear pathotype) affect P. pyrifolia (Japanese pears) (Tanaka, 1933; Simmons and Roberts, 1993). Chinese pears (Pyrus bretschneideri and Pyrus ussuriensis) are also affected in northeastern China (CABI, 2017). A. gaisen has not been shown to affect P. communis (European pear) or its hybrid P. × lecontei. Therefore, there is uncertainty whether European pear and its hybrid P. × lecontei are hosts of the small‐spored AK‐toxin producer Alternaria.

The EU legislation includes Cydonia in addition to Malus and Pyrus. Farr et al. (1989), based on Joly (1964), reported A. mali on Cydonia oblonga. However, Joly (1964) also considered A. mali to be synonymous with Alternaria citri and Alternaria chartarum, with the latter having a very wide host range among which species belonging to several families of poaceous and woody plants. Joly (1964) was most likely referring to small‐spored A. alternata‐like fungi detected on those plant species, including apples, and not to AM‐toxin producer Alternaria. Therefore, as no other literature could be found to support the host status of Cydonia, the Panel decided not to include this plant genus in the host range of the pests in this pest categorisation.

All the above‐mentioned hosts are regulated.

3.4.2. Entry

Is the pest able to enter into the EU territory? If yes, identify and list the pathways!

Yes, under the current EU legislation, the small‐spored AM/AK‐toxin producer Alternaria could potentially enter the risk assessment area via the dormant host plants for planting and the fresh fruit pathways

The PLH Panel identified the following pathways for the entry of the pests into the EU territory:

1. host plants for planting, including dormant plants, and

2. fresh fruit of host plants originating in infested Third countries.

No evidence exists for small‐spored AM‐/AK‐toxin producer Alternaria affecting Malus spp. and Pyrus spp. to be seed‐borne.

Although there is no quantitative data available, spores of the pests may be also present as contaminants on other substrates (e.g. non‐host plants, plant products and other objects) imported into the EU. Nevertheless, this is considered to be a minor pathway for the entry of small‐spored AM‐/AK‐toxin producer Alternaria into the risk assessment area.

Under the current EU legislation, the import of host plants for planting, excluding seeds and dormant plants, from non‐EU countries is prohibited. Therefore, only the host plants for planting at dormant stage and the fresh fruit pathways are relevant for the entry of the pests into the risk assessment area.

No data exists in Eurostat on imports of dormant host plants for planting from Third countries into the EU territory (Source: Eurostat, search done on 12/10/2017). The volume of apples and pears imported into the EU from non‐EU countries and continents infested with the AM‐ and AK‐toxin producer Alternaria is presented in Tables 8 and 9, respectively.

Table 8.

Total volume (in tons) of apples imported during the period 2011–2015 into the 28 EU Member States from non‐EU28 countries and from continents where AM‐toxin producer Alternaria are reported as present (Source: Eurostat, extracted on 12/10/2017)

Total EU 28 apple imports (in tons) from	2011	2012	2013	2014	2015
Non‐EU countries	595,914	504,178	668,796	495,034	455,291
Infested American countries	181,631	144,282	181,623	173,460	118,650
Infested Asian countries	5,699	3,459	7,921	2,552	1,182
Australia	275	480	469	95	699
Serbia	32,247	2,166	38,860	5,258	23,150
Turkey	127	127	302	166	222

Table 9.

Total volume (in tons) of pears imported during the period 2012–2015 into the EU Member States from non‐EU countries and from continents where AK‐toxin producer Alternaria are reported as present (Source: Eurostat, extracted on 12/10/2017). No import data available for 2011

Total EU 28 pear imports (in tons) from	2012	2013	2014	2015
Non‐EU countries	226,965	284,723	242,205	221,239
Infested Asian countries	11,583	10,397	6,418	9,536

No data available for Pakistan and Taiwan.

Based on the above data, during the period 2011–2015, 30–37% of the total volume of apples imported by the 28 EU MSs from Third countries originated in areas where AM‐toxin producer Alternaria are reported as present.

Based on the above data, during the period 2011–2015, 3–5% of the total volume of pears imported by the 28 EU MSs from Third countries originated in areas where AK‐toxin producer Alternaria are reported as present. However, no specific data exist in Eurostat on imports of P. pyrifolia, P. ussuriensis or P. bretschneideri fruit from infested Third countries into the EU.

There are no records of interception of Alternaria spp. in the Europhyt database (search done on 11 October 2017).

3.4.3. Establishment

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

Yes, both the biotic (host availability) and abiotic (climate suitability) factors suggest that small‐spored AM‐ and AK‐toxin producer Alternaria could potentially establish in the risk assessment area, similarly to other well‐established Alternaria species.

3.4.3.1. EU distribution of main host plants

Hosts of the small‐spored AM‐toxin producer Alternaria (i.e. Malus spp., P. communis) are widely distributed in the risk assessment area (Tables 10 & 11).

Table 10.

Area cultivated with apples in the EU between 2011 and 2015 (in 1,000 ha). Source: Eurostat, extracted on 28/8/2017

EU Member Statesa	2011	2012	2013	2014	2015	Mean of EU apple‐growing area (in 1,000 ha)
EU28	548.36	558.62	536.75	524.50	537.91	541.23
Poland	183.50	194.70	162.40	163.10	180.40	176.82
Romania	52.72	55.37	60.28	56.13	55.88	56.08
Italy	54.07	54.13	53.01	52.00	52.16	53.07
France	52.80	51.79	50.68	50.17	49.65	51.02
Hungary	33.09	32.04	33.36	33.26	32.80	32.91
Germany	31.76	31.74	31.74	31.74	31.74	31.74
Spain	31.51	30.79	30.79	30.73	30.72	30.91
United Kingdom	16.00	16.00	20.00	16.00	16.00	16.80
Portugal	12.54	12.90	13.66	13.85	14.01	13.39
Greece	13.48	12.47	12.93	12.26	11.76	12.58
Lithuania	10.11	11.83	11.67	11.27	10.68	11.11

^aOnly Member States growing more than 10,000 ha are reported.

Table 11.

Area cultivated with pears in the EU between 2011 and 2015 (in 1,000 ha) – Source: Eurostat, extracted on 28/8/2017

EU Member Statesa	2011	2012	2013	2014	2015	Mean of EU apple‐growing area (in 1,000 ha)
EU28	129.42	124.66	120.38	117.01	117.07	121.71
Italy	36.34	34.24	31.53	30.15	30.86	32.62
Spain	27.01	25.48	24.24	23.64	22.88	24.65
Portugal	10.97	11.23	12.01	12.01	12.12	11.67
Poland	11.70	10.90	9.50	9.20	9.20	10.10

^aOnly Member States growing more than 10,000 ha are reported.

There is no data concerning the abundance and distribution of the hosts of the small‐spored AK‐toxin producer Alternaria (i.e. Asian pears) in the risk assessment area, although enterprises producing plants for planting and fresh fruit of Japanese pears are currently present in the EU territory.

Apples are also grown, but to a lesser extent, in the Czech Republic, the Netherlands, Belgium, Austria, Croatia, Bulgaria, Slovakia, Latvia, Slovenia, Denmark, Sweden, Estonia, Cyprus, Ireland, Finland and Luxembourg.

Pears are also grown, but to a lesser extent, in Belgium, the Netherlands, France, Greece, Romania, Hungary, Germany, the United Kingdom, Croatia, the Czech Republic, Lithuania, Austria, Bulgaria, Denmark, Slovakia, Slovenia, Latvia, Sweden, Cyprus and Luxembourg.

3.4.3.2. Climatic conditions affecting establishment

Small‐spored Alternaria species have already been established in the EU and AM‐/AK‐toxin producer Alternaria have been detected in both southern and northern EU MSs (e.g. Italy, Denmark). In addition, the biology and epidemiology of small‐spored AM‐/AK‐toxin producer Alternaria is similar to that of other well‐established in the EU Alternaria. Therefore, the climatic conditions in the risk assessment area are not a limiting factor for the establishment of small‐spored AM‐/AK‐toxin producer Alternaria.

3.4.4. Spread

3.4.4.1. Vectors and their distribution in the EU

Is the pest able to spread within the EU territory following establishment? Yes

How? By natural and human‐assisted means

Small‐spored AM‐/AK‐toxin producer Alternaria can spread in the risk assessment area by both natural and human‐assisted means.

Spread by natural means. Long‐distance spread of Alternaria is likely by means of windborne conidia produced on symptomatic host plant tissues, whereas short‐distance spread (within a tree or between trees) is by water splash and/or wind‐driven rain carrying conidia. Conidial release is favoured by rain events or sudden changes in relative humidity (Rotem, 1994).

No information was found in the literature on the distance over which conidia of the pests can be carried by air currents.

Dispersion indices, two‐dimensional distance analysis and spatial autocorrelation analysis used to study the spatial distribution pattern of small‐spored AM‐toxin producer Alternaria (formerly A. mali) in apple orchards in the USA and Korea, suggested that arthropods may also be responsible for the introduction of inoculum into the orchards (Filajdić and Sutton, 1994; Filajdić et al., 1995a,b; OunHa et al., 1997).

Spread by human assistance. The pests can spread over long distances via the movement of infected host plants for planting (rootstocks, grafted plants, scions, etc.), including dormant plants and fresh fruits.

3.5. Impacts

Would the pests’ introduction have an economic or environmental impact on the EU territory?

Yes, the introduction of the pests could potentially cause yield and quality losses to Malus and Pyrus grown in the risk assessment area.

Alternaria leaf blotch and fruit spot of apple are economically important diseases in Southeast Asia, Southeast USA, Australia and northern Italy causing premature defoliation and fruit spotting (Filajdić and Sutton, 1991, 1992b; Rotondo et al., 2012; Harteveld et al., 2013; Sawamura, 2014). The disease mostly affects high‐value apple cultivars that are susceptible to the AM‐toxin, such as Golden Delicious, Red Delicious, Gala, Royal Gala, Fuji, Pink Lady, Indo, etc. (Filajdić and Sutton, 1991; Ferree and Warrington, 2003; Horlock, 2006; Rotondo et al., 2012). Leaf infection can result in 60–85% defoliation in susceptible cultivars (Filajdić and Sutton, 1992b; Jung, 2007). Fruit symptoms are usually limited to small, corky, dark lesions often associated with the lenticels. The disease may cause soft rot, especially on fruit already damaged by other means (Jung, 2007), such as mechanical injuries, red mites (Filajdić et al., 1995a,b), apple aphids (Filajdić et al., 1995b) or cracks around the calyx (Stern et al., 2013; Ginzberg et al., 2014). Affected fruits, if not dropped, are downgraded from premium fresh fruit to juice, resulting in significant financial losses to the growers (Persley and Horlock, 2009).

In addition to yield and quality losses of fruit, premature defoliation also depletes the carbohydrate reserves in the trees, giving rise to reduced tree vigour and productivity in the following seasons (Cordes, 1987; Suzuki et al., 1987).

Filajdić and Sutton (1991) reported that, during the summers of 1987 and 1988, the disease caused 60% defoliation of the variety Delicious in the apple‐growing areas of North Carolina, USA.

In Australia, the disease occurs in all apple‐growing regions causing yield losses of 15–25% in high value cultivars to the apple industry (Horlock, 2006; Harteveld et al., 2013). Severe leaf infection can result in 60–85% defoliation on susceptible apple cultivars (Persley and Horlock, 2009).

Severe outbreaks of Alternaria leaf blotch and fruit spot were recently observed in cv. Pink Lady apples in northern Israel, especially on fruit (Gur et al., 2017). Symptoms involved cracks and rot around the calyx and external fruit rot. Up to 80% of the fruit in some orchards were affected by the disease.

In northern Italy, Alternaria leaf blotch and fruit spot of apple cause damages that vary from 3–4% to 40% of the fruit showing symptoms (Anonymous, 2005; Antoniacci and Montuschi, 2006; Ortalda, 2006).

Black spot disease caused by small‐spored AK‐toxin producer Alternaria (as A. gaisen or A. kikuchiana or A. alternata f. sp. kikuchiana or A. alternata Japanese pear pathotype) is one of the most serious diseases of a limited number of cultivars of Japanese pear (P. pyrifolia) grown in Asia, including the commercially important cvs. Nijisseiki and Shinsui (Kohmoto et al., 1992; Tanaka, 1933; Nakashima et al., 1985; Otani et al., 1985; Terakami et al., 2016). Nevertheless, no quantified data on yield/quality losses could be retrieved from the literature.

Overall, there is uncertainty with respect to the contribution of small‐spored AM‐/AK‐toxin producer Alternaria on the impact caused by the small‐spored Alternaria detected on apples and pears worldwide, particularly for those reports where identification was based on morphological observations and pathogenicity tests, and not on the detection of the genes responsible for the biosynthesis of the AM‐ or the AK‐toxins.

The Panel considers that the introduction and spread of the pests in the risk assessment area could cause some impacts to apple and pear production, although their magnitude is unknown.

3.6. Availability and limits of mitigation measures

Are there measures available to prevent the entry into, establishment within or spread of the pest within the EU such that the risk becomes mitigated?

Yes, the likelihood of pest entry can be mitigated if host plants for planting (including dormant plants) and fresh fruit are sourced from pest‐free areas or pest‐free places of production and are inspected and lab tested for the detection of the AM‐ or AK‐toxin biosynthesis genes both at the place of origin and the EU entry point. In infested areas, sanitation, agricultural practices, including resistant cultivars, and fungicide sprays are available for disease management.

Measures for preventing the entry of the pests into the risk assessment area include:

• sourcing host plant material, including dormant plants and fruit, from pest‐free areas or pest‐free places of production

• phytosanitary certificate for the export of host plants for planting and fruit from infested countries

• inspection and testing of host plants for planting and fruit prior to export to the EU and at the EU entry point.

Measures for preventing the establishment and spread of the pests in the risk assessment area include:

• use of resistant host varieties

• use of sanitary measures (e.g. removal of infected plants or plant parts and pruning residues, disinfection of pruning and grafting tools)

• application of fungicide sprays

• crop residue management

• restrict the movement of infected plant material.

3.6.1. Biological or technical factors limiting the feasibility and effectiveness of measures to prevent the entry, establishment and spread of the pest

The following biological and technical factors could potentially limit the feasibility and effectiveness of measures to prevent the entry into, establishment and spread within the risk assessment area of small‐spored AM‐ or AK‐toxin producer Alternaria:

• The similarity of disease symptoms and colony and conidial morphology of the pests with those of other small‐spored Alternaria species affecting apples and pears worldwide and not carrying the genes for the AM‐ or AK‐toxin biosynthesis makes impossible the detection/identification of the pests based only on symptomatology and cultural/morphological characters.

• Methods for the detection and identification of small‐spored Alternaria carrying the genes for the AM‐ or AK‐toxin biosynthesis are available but difficult to be implemented on a large scale.

3.6.2. Control methods

In the infested areas, the following agricultural practices and sanitary and chemical measures are used for the management of the diseases caused by small‐spored AM‐/AK‐toxin producer Alternaria on Malus spp. and Pyrus spp. (CABI, 2017):

• Agricultural measures:

  • 1–  Use of resistant cultivars (Sawamura, 2014; Shin et al., 1986; EPPO, 2017; Machida et al., 1984; Kim et al., 1985; Kozaki, 1987).
  • 2–  Improve orchard ventilation by adequate tree spacing, row orientation and pruning.

• Sanitation measures to reduce inoculum sources in the orchards (e.g. burial of fallen infected leaves, removal of symptomatic fruit) (CABI, 2017).

• Chemical control is achieved using fungicides such as iprodione, mancozeb and captan (although some isolates have developed resistance to some of these fungicides) (Lee and Kim, 1986; Osanai et al., 1987; Asari and Takahashi, 1988). In Japan, the disease requires specific and regular fungicide sprays. Applications of protectant fungicides are made after petal fall (Sekita et al., 1994). Only iprodione was found to be effective for the control of the disease in North Carolina (USA) (Filajdić and Sutton, 1992a). Captafol (Adachi and Fujita, 1984) and guazatine (Yagura et al., 1984) are also used for disease management in the infested areas. However, these two fungicides are not authorised in the EU.

3.7. Uncertainty

1. Pest distribution: There is uncertainty with respect to the distribution of the pests worldwide and in the risk assessment area, particularly for those reports where identification was based on morphological observations and pathogenicity tests, and not on the detection of the genes responsible for the biosynthesis of the AM‐ or the AK‐toxin.

2. Host range: There is uncertainty whether P. communis (European pear) or its hybrid P. x lecontei are hosts of the small‐spored AK‐toxin producer Alternaria.

3. Entry: The absence of data regarding the quantity of dormant host plants for planting imported from affected non‐EU countries into the risk assessment area.

4. The absence of data regarding the abundance and distribution of P pyrifolia, the host of the small‐spored AK‐toxin producer Alternaria, in the EU28 and on the susceptibility of the grown cultivars; this uncertainty affects entry (transfer of the pests from the pathway of entry to the host grown in the risk assessment area), establishment, spread and impact.

5. Spread: The maximum distance the conidia of the pests could travel by air currents due to lack of knowledge

6. Impacts: The contribution of small‐spored AM‐/AK‐toxin producer Alternaria on the impact caused worldwide by small‐spored Alternaria pathogenic to apples and pears is uncertain.

4. Conclusions

Small‐spored AM‐/AK‐toxin producer Alternaria do not meet all the criteria assessed by EFSA for consideration as potential quarantine pests or regulated non‐quarantine pests for the EU territory (see Table 12).

Table 12.

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	Panel's conclusions against criterion in Regulation (EU) 2016/2031 regarding Union regulated non‐quarantine pest	Key uncertainties
Identity of the pest (Section  3.1 )	The identity of the pests is clearly defined and there are reliable methods for their detection and identification	The identity of the pests is clearly defined and there are reliable methods for their detection and identification	None
Absence/presence of the pest in the EU territory (Section  3.2 )	Small‐spored AM‐toxin producer Alternaria are reported in Italy and Denmark, whereas small‐spored AK‐toxin producer Alternaria are reported in France, Hungary, Italy and Portugal. Based on available information, the pest distribution is currently restricted.	Small‐spored AM‐toxin producer Alternaria are reported in Italy and Denmark, whereas small‐spored AK‐toxin producer Alternaria are reported in France, Hungary, Italy and Portugal. Based on available information, the pest distribution is currently restricted.	There is uncertainty about the distribution of the pests in the risk assessment area, particularly where the presence of AM‐/AK‐toxin genes has not been tested (Uncertainty 1).
Regulatory status (Section  3.3 )	Small‐spored AM‐/AK‐toxin producer Alternaria are currently officially regulated as quarantine pests on Cydonia Mill., Malus Mill. and Pyrus L., other than seeds, originating in non‐European countries (Dir 2000/29/ EC).	Small‐spored AM‐/AK‐toxin producer Alternaria are currently officially regulated as quarantine pests on Cydonia Mill., Malus Mill. and Pyrus L., other than seeds, originating in non‐European countries (Dir 2000/29/ EC).	None
Pest potential for entry, establishment and spread in the EU territory (Section  3.4 )	Small‐spored AM‐/AK‐toxin producer Alternaria could potentially enter, become established, and spread within the EU. Pathways of entry: 1. Host plants for planting, excluding seeds but including dormant plants, and 2. Fresh fruit of host plants	Small‐spored AM‐/AK‐toxin producer Alternaria could potentially spread in the EU through movement of host plants for planting, fresh fruits of host plants, and natural means (airborne conidia). Therefore, plants for planting is a main means of spread, but not the only one.	Uncertainty on the host range of the small‐spored AK‐toxin producer Alternaria (Uncertainty 2) Absence of data on dormant host plants for planting imported from affected non‐EU countries into the risk assessment area (Uncertainty 3) Uncertainty about the abundance/distribution of Pyrus pyrifolia in the EU28 and on the susceptibility of the grown cultivars (Uncertainty 4) Uncertainty about the maximum distance, the conidia of small‐spored AM‐/AK‐toxin producer Alternaria could travel by air currents (Uncertainty 5)
Potential for consequences in the EU territory (Section  3.5 )	The introduction and spread of the pests in the EU could cause yield and quality losses in apple and pear production, but the magnitude of the impact is unknown.	The presence of the pests on host plants for planting could have a negative impact on their intended use	The contribution of small‐spored AM‐/AK‐toxin producer Alternaria on the impact caused worldwide by small‐spored Alternaria pathogenic to apples and pears is uncertain (Uncertainty 6)
Available measures (Section  3.6 )	Phytosanitary measures are available to prevent the entry of the pests into the EU (e.g. sourcing host plants for planting and fruit from pest‐free areas or pest‐free places of production). Inspection at the place of origin and at the EU entry point is not fully effective to prevent the entry of the pests. There are no fully effective measures to prevent establishment and spread	There are no fully effective measures to prevent the presence of the pests on host plants for planting
Conclusion on pest categorisation (Section  4 )	To the best of the Panel's knowledge, small‐spored AM‐/AK‐toxin producer Alternaria are not under official control in those restricted areas where they have been found. As such, the pests do not meet all the criteria evaluated by EFSA.	Small‐spored AM‐/AK‐toxin producer Alternaria can spread by movement of infected fruits, as well as by airborne conidia; therefore, they do not meet all the criteria assessed by EFSA.	There is uncertainty about the distribution of the pests in the risk assessment area, particularly where the presence of AM‐/AK‐toxin genes has not been tested (Uncertainty 1).
Aspects of assessment to focus on/scenarios to address in future if appropriate	Given that all the data available in the literature have been explored, the Panel considers that a survey could be carried out using appropriate pest identification methods (see Section 3.1.3) to define the current geographical distribution and impact of small‐spored AM‐/AK‐toxin producer Alternaria in the risk assessment area before a full PRA is performed to reduce the uncertainty related to the conclusion of this pest categorisation.

Abbreviations

DG SANCO

Directorate General for Health and Consumers

EPPO

European and Mediterranean Plant Protection Organization

FAO

Food and Agriculture Organization

HST

host‐specific toxin

IPPC

International Plant Protection Convention

MS

Member State

PLH

EFSA Panel on Plant Health

TFEU

Treaty on the Functioning of the European Union

ToR

Terms of Reference

Suggested citation: EFSA PLH Panel (EFSA Panel on Plant Health) , Jeger M, Bragard C, Caffier D, Candresse T, Chatzivassiliou E, Dehnen‐Schmutz K, Gilioli G, Grégoire J‐C, Jaques Miret JA, MacLeod A, Navajas Navarro M, Niere B, Parnell S, Potting R, Rafoss T, Urek G, Van Bruggen A, Van der Werf W, West J, Winter S, Vicent A, Vloutoglou I, Bottex B and Rossi V, 2017. Scientific Opinion on the pest categorisation of small‐spored Alternaria carrying the genes for the AM‐ or AK‐toxin biosynthesis. EFSA Journal 2017;15(12):5099, 27 pp. 10.2903/j.efsa.2017.5099