Ref. Ares(2018)5819641 - 14/11/2018

EUROPEAN COMMISSION DIRECTORATE-GENERAL FOR HEALTH AND FOOD SAFETY

Health and food audits and analysis

DG(SANTE) 2018-6485

FINAL REPORT OF AN AUDIT CARRIED OUT IN FROM 28 MAY 2018 TO 01 JUNE 2018 IN ORDER TO EVALUATE THE SITUATION AND OFFICIAL CONTROLS FOR XYLELLA FASTIDIOSA

In response to information provided by the competent authority, any factual error noted in the draft report has been corrected; any clarification appears in the form of a footnote. Executive Summary This report describes the outcome of an audit carried out by the Directorate-General for Health and Food Safety of the European Commission in Italy from 28 May to 1 June 2018. The objective of the audit was to evaluate the situation of Xylella fastidiosa (Xf) and in particular, the implementation of Commission Implementing Decision 2015/789/EU of 18 May 2015 (the Decision) setting out protective measures for its control. Although there is structured multichannel awareness-raising activity in the Region, it does not have the intended effect towards non-professional olive growers, interest groups and the general public for counteracting the negative impact of inaccurate or misleading information related to Xf, which is currently present in the region. The rate of false negative results obtained by the ELISA tests raises serious concerns as the undetected infected host plants in the demarcated area (DA) significantly compromise the control measures, in particular the eradication in the buffer zone. The survey method applied in the DA during the 2016 and 2017 annual campaigns was generally in line with the Decision. However, as part of the visual inspections were carried out in periods not suitable for the detection of the key symptoms appearing on the leaves of deciduous and herbaceous host, many infected plants could remain undetected. Although all host plants which tested positive in the '20km zone' during the 2016 surveillance campaign had been removed at the time of the audit, the excessive delays in felling favoured the continuous spread of the pathogen during the 2017 flight period of the vector. Following the 2017 survey campaign, in the Buffer Zone, the eradication measures were only partially implemented and in the '20km zone' only 10.7% of the more than three thousand detected positive olive trees had been removed at the time of the audit. The lack of actions at national level to either grant a derogation or to speed up the procedures required by the national legislation for the implementation of the eradication and containment measures in areas subject to national protection measures cause significant delays in the removal of infected plants. Court appeals prevent the implementation of certain actions. Difficulties in the identification of the owners and shortages in administrative capacities contributed to the delays in the removal of infected plants. Unless urgent actions are taken, these issues are likely to continue as impeding factors in the future. As a result of these shortcomings the protective function of the BZ is compromised and at least a part of the '20km zone' cannot sustain its intended function as a barrier against the spread of the disease. In particular, due to the high number of infected trees not removed until after the start of the 2018 flight period of the vector, a rapid northward spread of the disease is expected in 2018. The agricultural practices which were made obligatory by the Italian authorities in the DA for the management of Xf and its vectors would, if properly implemented, assist significantly in the containment. However, the efficiency is compromised by the partial implementation in the DA. The currently applied movement control measures provide very limited guarantees that specified plants do not leave the DA, including for other EU Member States. The report contains recommendations to the National Plant Protection Organisation of Italy to address the shortcomings identified.

I Table of Contents 1 Introduction...... 1 2 Objectives and scope...... 1 3 Legal Basis...... 2 3.1 Relevant EU Legislation/measures...... 2 3.2 International standards...... 2 4 Background ...... 2 4.1 Situation of Xylella fastidiosa in the EU ...... 2 4.2 Situation of Xylella fastidiosa in Italy...... 3 4.3 Previous audits...... 4 5 Findings and Conclusions ...... 5 5.1 Organisational aspects of the plant health controls ...... 5 5.2 Surveys for the detection of Xylella fastidiosa in the demarcated area...... 11 5.3 Eradication measures...... 17 5.4 Containment measures...... 21 5.5 Appropriate agricultural practices ...... 25 5.6 Movement control of specified plants ...... 26 6 Overall Conclusions ...... 28 7 Closing Meeting...... 29 8 Recommendations ...... 29

II ABBREVIATIONS AND DEFINITIONS USED IN THIS REPORT

Abbreviation Explanation ARIF Regional Agency for Irrigation and Forestry, Region Apulia (Agenzia Regionale per le attività Irrigue e Forestali) BZ Buffer Zone as referred to in Article 4(2)(d) of the Decision CA Competent Authority CJEU Court of Justice of the European Union CNR National Research Council (Consiglio Nazionale Delle Ricerche), Institute for Sustainable Plant Protection, Bari CUFAA Command of Forest, Environment and Agri-food Units of the Carabinieri (Comando unità forestali, ambientali e agroalimentari) DA Demarcated Area as referred to in Article 4 of the Decision 'The Decision' Commission Implementing Decision (EU) 2015/789 of 18 May 2015 as regards measures to prevent the introduction into and the spread within the Union of Xylella fastidiosa DG Health and Food European Commission's Directorate-General for Health and Food Safety Safety ELISA Enzyme Linked Immunosorbent Assay EPPO European and Mediterranean Plant Protection Organisation EU European Union Host plant Plants for planting other than seeds belonging the genera and species listed in the Commission database of plant susceptible to Xf in the EU territory, as referred to by Article 1(b) of the Decision IPPC International Plant Protection Convention ISPM International Standards for Phytosanitary Measures IZ Infected Zone as referred to in Article 4(2) of the Decision LAMP Loop mediated isothermal amplification MIPAAF Ministry of Agriculture, Foodstuffs and Forest Policies (Ministro delle politiche agricole alimentari e forestali) Monumental tree Olive tree with historic, cultural, social or scientific value as referred to by Articles 6(2) and 7(7) of the Decision MLST multi locus sequence typing NPPO National Plant Protection Organisation RT-PCR Real time polymerase chain reaction RPS Regional Plant Health Service (Osservatorio fitosanitario regionale) Soprintendenza Cultural Heritage and Landscape Service of the Ministry of Cultural Heritage and Activities and Tourism (Soprintendenza archeologia, belle arti e paesaggio; Ministero dei beni e delle attività culturali e del turismo) Specified plant Host plants and other plants for planting other than seeds, as referred to in Article 1(c) of the Decision and belonging to the genera and species listed in Annex I of the Decision TAR Administrative Court for the Region (Tribunale amministrativo regionale) – an administrative court dealing with issues related to the implementation of regional legislation. The TAR for the Region Lazio is dealing with issues related to the implementation of national legislation at regional level. '20km zone' A location within the IZ within a distance of 20 km from the border of that zone with the rest of the Union territory, as referred to in Article 7(7)(c) of the Decision Xf Xylella fastidiosa

III 1 INTRODUCTION

This audit took place in Italy from 28 May to 1 June 2018 as part of the published audit programme of the Directorate General for Health and Food Safety of the European Commission (DG Health and Food Safety). The audit team consisted of two auditors and two legal experts of DG Health and Food Safety. Representatives of the Ministry of Agriculture, Foodstuffs and Forest Policies (MIPAAF) accompanied the audit team during the audit. An opening meeting was held on 28 May 2018 at the headquarters of the Regional Plant Health Service of Apulia (RPS) in Bari, with representatives of the MIPAAF, the Agricultural Directorate of the regional administration and RPS, during which the objectives and itinerary for the audit were confirmed and additional information necessary for the conduct of the audit was requested. Unless specified otherwise, the data quoted in the following sections and elsewhere in the report, was provided by the MIPAAF or the RPS.

2 OBJECTIVES AND SCOPE

The objective of the audit was to evaluate the situation of Xylella fastidiosa (Xf) and to analyse the legislative and administrative measures implemented for its control, in particular, the implementation of Commission Implementing Decision 2015/789/EU of 18 May 2015, as regards measures to prevent the introduction into and the spread within the Union of Xylella fastidiosa (Well and Raju) (the Decision). To meet the objective the following meetings and visits were carried out:

Meetings, visits No. Comments Competent Central 1 Ministry of Agriculture, Foodstuffs and Forest Authorities Policies Regional 4 Agricultural Directorate of the Regional (in Apulia) Administration Legal Service of the Regional Administration Regional Plant Health Service Forest, Environment and Agri-food Unit of the Carabinieri Plant health Surveillance 5 In the buffer zone and '20km zone', around control sites eradication and containment sites Eradication 3 Outbreak sites in the buffer zone Containment 2 Outbreak sites in the '20km zone' Movement control 1 Port Stakeholders 3 Growers, grower associations, nursery associations, environmentalist groups, researchers

The audit focused on the implementation of the relevant provisions of the Decision, in particular the surveillance, eradication and containment measures in the demarcated area (DA) in Apulia and the controls on movement of specified plants within and from the DA.

1 3 LEGAL BASIS

The audit was carried out under the general provisions of EU legislation, in particular Articles 21 and 27(a) of Council Directive 2000/29/EC, and in agreement with MIPAAF.

3.1 Relevant EU Legislation/measures

Council Directive 2000/29/EC provides for protective measures against the introduction into and spread within the EU of organisms harmful to plants or plant products. The Decision provides for detailed rules related to findings or outbreaks of Xf. The Decision defines the terms 'host plant' and 'specified plant' in relation to Xf and the applicable measures. Specified plants are listed in Annex I of the Decision and the list of host plants is published in a Commission database: (https://ec.europa.eu/food/plant/plant_health_biosecurity/legislation/emergency_measures/xylella- fastidiosa/susceptible_en). All EU legislation/measures referred to in this report are listed in Annex 1. References to legislation/measures are to the latest amended version, where applicable.

3.2 International standards

Article X (4) of the International Plant Protection Convention (IPPC) establishes that contracting parties should take into account, as appropriate, international standards when undertaking activities related to the Convention. The Decision makes reference to certain International Standards for Phytosanitary Measures (ISPMs) issued by the IPPC. The ISPMs of particular relevance to this audit are listed in Annex 2. Their full text is available on the IPPC website (www.ippc.int).

4 BACKGROUND

4.1 Situation of Xylella fastidiosa in the EU

Xf is one of the most dangerous plant bacteria worldwide, causing a variety of diseases, with significant economic impact for agriculture and the environment. The bacterium lives in the plant xylem tissue and blocks the flow of liquids in it. It is normally spread by spittlebugs, cicadas and sharpshooters which feed on fluids from the plant xylem. Approximately 300 plant species are susceptible to the bacterium worldwide, although not all of these plants show disease symptoms and not all plant species are affected by all of its four subspecies (fastidiosa, multiplex, pauca, and sandyi). Currently no measures are known to cure infected plants in open field. Xf was reported for the first time in the EU territory by the Italian Authorities in October 2013, in the Region of Apulia. Outbreaks were subsequently detected in France (2015), Germany (2016) and in Spain (2016-2018). The German outbreak has recently been formally confirmed as eradicated. Detailed information about the Xf situation in the EU is available on the website of the DG Health and Food Safety. (https://ec.europa.eu/food/plant/plant_health_biosecurity/legislation/emergency_measures/xylella-fastidiosa_en).

2 4.2 Situation of Xylella fastidiosa in Italy

Xf subspecies pauca was detected in 2013 in the Region of Apulia, in an area around the town of Gallipoli on olive trees. Since then, the disease has been spreading rapidly. In 2015 the entire territory of the Province of Lecce was declared as an infected zone (IZ) and in 2016- 2017 the bacterium reached parts of the Provinces of Brindisi and . Numerous plant species were found infected by the Xf subspecies pauca in the IZ, the vast majority of infected plants were olive trees. No reliable data are available regarding the total number of infected plants in the IZ as official surveys only concentrate on the 20 km part of that zone from the border with the rest of the EU territory ('20km zone'). Very large numbers of olive trees show symptoms of decline with differing levels of loss in productivity. Many infected trees are in severe decline or are already dead. Philaenus spumarius (meadow froghopper) - a very common, polyphagous and abundant spittlebug on olive trees - is known to be the main vector responsible for the transmission of the bacterium. The adults transmit the bacterium during their flight period while hopping and feeding on different plants and predominantly on olive trees. Scientific studies carried out in Apulia established that the flight period of the vector starts late April early May and lasts until late November. The first Commission Implementing Decision to combat Xf was adopted in February 2014, and refined in July 2014. In May 2015 the Decision introduced stricter rules on the basis of the pest risk assessment of the European Food Safety Authority. Since 2015 the Decision was amended three times (in December 2015, in May 2016 and again in December 2017). These amendments, among other elements, took into account the rapid spread of the pest towards the north of the region and the resultant need for the adjustment of the DA borders and of certain control measures. The current provisions require Italy to apply eradication measures in the 10km wide buffer zone (BZ), established from the borders of the IZ, and containment measures in the IZ, including specific reinforced measures in the '20km zone'. In the absence of any known method to cure the disease, the timely identification and immediate destruction of infected plants is considered a critical element of the eradication and/or containment strategy. At national level, Italy declared a state of emergency in February 2015. It was declared for 180 days and was prolonged once to the maximum allowed for by Italian law at the time, and was lifted subsequently in February 2016. During the state of emergency a special commissioner was appointed by MIPAAF to coordinate the eradication and containment measures in the region and to liaise with the relevant national authorities. In addition, state funds were allocated for controlling the outbreak. Following the lifting of the state of emergency, the implementation of the control measures is primarily the responsibility of the Region Apulia. In 2015 some growers appealed against the felling orders issued by the RPS n respect of infected host plants detected on their properties. The Administrative Court for the Lazio Region (TAR) suspended the implementation of the eradication measures and in February 2016 submitted a request for a preliminary ruling to the Court of Justice of the European Union (CJEU) on the validity of the Decision with regard to EU law. The CJEU issued its judgment in joined cases C-78/16 and C-79/16 on 9 June 2016, confirming the validity of the Decision and in particular of the obligation of the Member State concerned to immediately

3 remove, within a radius of 100 m around the plants which have been tested and found to be infected by the specified organism, host plants, regardless of their health status.. In the context of a criminal investigation, on 28 December 2015, the Prosecutor of Lecce issued a seizure order, which resulted in the suspension of the destruction of olive trees in relation to the Xf outbreak, even if the proprietor volunteered to do it. In the light of the CJEU judgment, this ban was revoked on 27 July 2016 clearing the way for the RPS to resume the application of the provisions of the Decision. Due to the continued non-compliance by Italy with the Decision, specifically as regards the removal of plants and survey activities in Apulia, and the ongoing rapid spread of the disease, the Commission launched formal infringement proceedings against Italy on 10 December 2015 to which Italy answered on 10 February 2016. As the Decision was meanwhile amended and given that the Italian authorities had failed to comply with this amended Decision as well, the Commission sent an additional letter of formal notice to Italy on 25 July 2016. In their response to the additional letter of formal notice on 26 August 2016 the Italian authorities indicated that, following the removal of the judicial obstacles, their activities in relation to fighting Xf had resumed. Based on the information provided by Italy, a Reasoned Opinion was sent to the Italian Authorities on 14 July 2017. Italy responded on 14 September 2017. The Commission concluded that, notwithstanding the efforts made, the situation in Italy continued to deteriorate and therefore decided to refer the case to the CJEU on 17/05/2018.

4.3 Previous audits

The Commission has carried out five audits to assess the situation of Xf and the official controls carried out by the Italian authorities (in February 2014, November 2014, June 2015, November 2015 and November 2016). The reports of these audits are available on the website of the DG Health and Food Safety (http://ec.europa.eu/food/audits- analysis/audit_reports/index.cfm). Each audit report highlighted considerable deficiencies in the implementation of the relevant EU legislation and concluded that without the proper implementation of the EU measures there was a pronounced risk for further spread of the disease. The report of the 2016 audit concluded that there had been positive developments regarding surveillance. However, it found that long delays in felling positively tested olive trees provided good opportunities for the spread of the pathogen during the flight period of the vector in 2016. It was considered that this situation would continue if action were not taken to remove all positive tested plants prior to re-emergence of the vector. The report also stated that operational challenges would arise for felling large numbers of olive trees and in particular for 'monumental' trees. The Italian Competent Authorities did not send comments on any of the five draft audit reports and did not provide action plans to address the recommendations made in any of these reports. However, since 2015 the annual action plans, prepared by the Region Apulia, and endorsed by the central competent authorities, dealt indirectly with some of the issues raised by the audit reports.

4 5 FINDINGS AND CONCLUSIONS

5.1 Organisational aspects of the plant health controls

Legal requirements Articles 1 and 2 of Directive 2000/29/EC, in particular provisions relating to the organisational aspects of plant health controls.

Article 3a (contingency plans), Article 6(8) (public awareness), Article 13a (awareness campaigns) and Article 14 (reporting on measures) of the Decision.

Findings

5.1.1 Competent authorities

1. The organisational aspects of plant health controls in Italy are described in sections 1 and 2.11 of the DG Health and Food Safety country profile for the country (http://ec.europa.eu/food/audits-analysis/country_profiles/details.cfm?co_id=IT) and in the previous audit reports. In summary: MIPAAF is the Single Authority for plant health in Italy. At central level it is responsible for plant health policy and coordination of the relevant activities of the regions. Plant health responsibilities are assigned to the regions. The relevant bodies of the regional administrations are directly responsible for the implementation of controls. 2. In Apulia, the Agricultural Directorate of the regional administration is responsible for Xf controls and the measures are mainly implemented by the RPS. Certain related official controls are carried out by the Command of Forest, Environment and Agri- food Units of the Carabinieri (CUFAA). The surveillance in the DA is implemented by the Regional Agency for Irrigation and Forestry (ARIF).

5.1.2 National and regional legislation

3. The Decree of 18 February 2018 of the Minister for Agriculture, Foodstuffs and Forest Policies on “Emergency measures for the prevention, the control and the eradication of Xylella fastidiosa (Well et al.) in the territory of the Italian Republic” defines the phytosanitary measures to be taken following the outbreak of the bacterium. It repeals the Decree 7 December 2016. In Annex II it lists the municipalities belonging to the IZ. Section IV of the Annex lists the specific measures intended to manage the Xf outbreak in Apulia (soil tilling, vector control). However, no detailed measures with deadlines are laid down concerning the removal of infected plants and surveys. 4. Regional Law of No 4 of 29 March 2017 implements plant health measures to prevent and contain the spread of Xf and specifies measures to protect the landscape, environment, health, identity and the economy of the areas affected. 5. Regional Law No 37 of 20 September 2017 provides for interpretation of certain articles of the Regional Law of 29 March 2017, regarding the implementation of eradication measures, the financial support to nurseries and the isolation measures for 'monumental trees'. 6. Regional Law No. 64 of 22 December 2017 established a general derogation to the regional provisions on constraints on forestry, environmental, hydrogeological and

5 landscape for the implementation of eradication and containment measures in such areas. It also determines that the mandatory phytosanitary measures adopted by RPS shall be immediately implemented by owners. 7. Regional Act DDS 109 of 19 March 2018 of the Agriculture, Rural Development and Environment Directorate amended the borders of the BZ after positive olive trees were identified in that zone (see chapter 5.3.1). 8. The National Contingency Plan for managing Xf in Italy is published as an annex of the Decree of 18 February 2018 of the Minister Agriculture, Foodstuffs and Forest Policies. The audit team noted that the plan deals with all aspects listed in Article 3a(2) of the Decision. 9. The Regional Action Plan for 2017 was approved on 5 May 2017. It contains a detailed description of the measures regarding monitoring, eradication, containment and phytosanitary controls and allocates regional funds for their implementation.

5.1.3 Issues derived from Italian legislation, which influence the implementation of the Decision

10. The Italian competent authorities (CA) informed the audit team that national and regional legal constraints cause delays in the implementation of the eradication and containment measures, in particular the removal of positively tested plants and the clear-cut around them. In the current BZ and in the '20km zone' there are areas which are subject to national legislation for landscape and nature conservation, as well as regional legislation for forest and water resource management and nature conservation. The CA indicated that constraints relate to:  'National and regional protected areas' as defined by law 6 December 1991, n. 394 and regional law 24 July 1997, n. 19;  'Hydrogeological areas' as defined by Royal Decree 30 December 1923, n. 3267;  'Further Landscape Contexts', as defined by the Regional Landscape Plan of Region Apulia (Article 143(1) lett. e) of legislative decree n. 42 of 22 January 2004 – the so called “Code of Cultural Heritage and Landscape;  'Landscape assets', as defined by the Regional Landscape and Territory Plan of Apulia (Article 134 of legislative decree n. 42 of 22 January 2004 – so called “Code of Cultural Heritage and Landscape”);  'Hydraulic hazardous areas, geomorphological hazardous areas and areas at risk', as defined in the Basin management Plan of the Region Apulia (Article 17 ter (6) of law 18 May 1989, n. 183). 11. As a general rule, in areas subject to national and regional legislation, any intervention with potential impact on the protected status of the sites, would require an authorisation by the competent regional or national authority. 12. The audit team noted that at the time of the audit within the BZ and the '20km zone' there were no positive plants situated in areas protected under Directive 92/43/EEC on the conservation of natural habitats and of wild fauna and flora (Natura 2000). 13. In relation to the areas subject to regional constraints, Apulia adopted the Regional law of Apulia No. 64 of 22 December 2017. This act establishes a general derogation to the regional rules in order to facilitate the implementation of the EU measures without specific authorisations. The legality of this law establishing such general derogation

6 has been challenged before the TAR by owners of olive trees subject to RPS felling orders. 14. In areas subject to national constraints, any removal of trees and shrubs requires a prior positive assessment by the Italian Cultural Heritage and Landscape Service (Soprintendenza). This is a lengthy and laborious process (see chapters 5.3.2 and 5.4.1). 15. At national level, no derogation or legal arrangement has been adopted in relation to the direct application of the EU measures. Consequently, the Region has to prepare a landscape report for the Soprintendenza on the host plant removal activity for each of the areas subject to national constraints. The report has to clearly identify all the trees subject to felling orders. The Region is only in a position to proceed with removal of infected plants when the plan is positively assessed and the intervention is authorised. 16. The completion of the eradication measures in the BZ is delayed if the owner invokes a 'monumental tree' derogation provided by Article 6.2a of the Decision. (Negatively tested host plants with a historical value (i.e. 'monumental' olive trees) may not be subject of felling in the 100m area around the positives, provided that they are physically protected.) In Apulia, regional legislation defines the criteria, under which an olive tree may be considered as 'monumental' and establishes a regional register (regional law n. 14 of 4 June 2007). The register currently contains 55,650 olive trees defined as monumental. The RPS estimates that about 10% of trees in the BZ could be classified as 'monumental'. Upon request of the owner, the RPS assesses, case-by-case, whether a non-infected olive tree in the clear-cut area is 'monumental' or not. At the time of the audit there were three appeals before the TAR, presented by 11 separate owners, challenging the RPS assessment of 'non-monumental' trees. 17. At the time of the audit, the direct application of EU measures was subject to several legal challenges mainly related to the validity of the administrative orders for removal. According to the national Italian legislation in force, upon request of the claimant, the Court may suspend the effect of removal order as an interim measure. In such a case, the RPS cannot implement the measures until the appropriate legal processes related to the challenges are completed. 18. The RPS also informed the audit team that additional legal issues might arise in future cases, when the owner does not remove the infected plants himself within the 15 days allocated by the RPS order. Under such situations, ARIF, under the order of the RPS, will carry out the felling. The access to and work on a private property without the owner's consent give rise to additional legal issues.

5.1.4 Communication and cooperation within the plant health services and with other authorities

19. MIPAAF maintains regular contacts with the regions on plant health issues and plays a coordination and advisory role in the elaboration of control measures. The exchange of information takes place mainly by electronic means. RPS representatives have monthly meetings with MIPAAF. 20. In 2017-2018 MIPAAF initiated some discussions with other relevant national authorities to address the delays in the removal of infected host plants and the clear-cut around them as appropriate, result from the application of the procedures established

7 under national environmental and heritage protection legislation (see also chapter 5.1.3). However, no agreement or resolution has been reached and no derogation has been adopted at national level to speed-up the procedures. 21. The audit team noted that the implementation of the EU measures in Apulia is benefitting from strong cooperation between the regional competent authorities involved. The regional authorities also maintain close working relations with CUFAA (see also chapter 5.6.2).

5.1.5 Awareness raising relating to Xf

22. There are awareness raising campaigns Apulia as requested by Article 13a of the Decision. The main information source is an official internet portal for Xf (www.emergenzaXylella.it), operated jointly by MIPAAF and the authorities in Apulia. It contains regularly updated information about the EU, national and regional legislation, specified plants, scientific evidence about the bacterium and the disease, materials used for the training of phytosanitary agents engaged in monitoring, monitoring data, action plans and survey plans, as well as maps on the outbreak situation. It also contains results of the confirmatory laboratory tests and the number and location of the olive trees, which have been tested positive and of those trees which have been removed. 23. In Apulia, the regional administration has made efforts to inform the general public and interested parties about the latest developments related to Xf.  The Agricultural Directorate of the Region and the RPS maintain close relations with the regional media and professional associations. Different means, such as press releases, general and targeted communications, meetings with the interested parties are used to disseminate information;  The regional authorities also maintain good relations with research institutions and universities, which are involved in Xf related research. These organisations also help in disseminating information and raising awareness;  RPS and CUFAA staff, as well as ARIF agents, maintain close working relations with olive growers, nurseries, professional associations and municipalities. Meetings are organised regularly to collect and disseminate information. During the field visits, the inspectors and agents provide up-to-date information to the stakeholders about the outbreak situation;  The RPS recently published a poster and has displayed it in ports, railway stations, petrol stations and airports to inform travellers and the general public. The poster indicates the borders of the different zones of the DA, describes the disease and indicates the danger of the spread. It further informs against the movement of susceptible plants out of the DA. 24. The audit team met olive growers, professional associations, non-governmental organisations and lobby groups representing different types of interest and noted that:  Professional olive growers are fully aware of the risk and economic consequences of the spread of the disease. They are committed to cooperate with the authorities in implementing appropriate measures, including the felling of infected plants in order to protect their olive groves;  The olive production area in Apulia is a patchwork of professionally maintained groves, and small olive plots owned by non-professionals. The audit team considers that in particular the non-professional olive growers and the general public do not to have sufficient information about the situation and the risk. The non-professional

8 olive growers are divided concerning the necessity of felling olive trees for protective reasons. They do not have the necessary resources either for the implementation of appropriate agricultural measures and;  Numerous organisations and interest groups are active in the region, which in the view of the RPS, are the source of certain unjustified and inaccurate information about the disease and its management. The RPS stated that the main aim of these organisations is to prevent any olive tree felling. The main arguments concentrate on the immediate economic and environmental impact of cutting olive trees, while the long-term effect of the rapid spread of the disease is not considered;  The information provided by the regional authorities during the awareness raising activity competes with scientifically inaccurate information spread by organisations mentioned above and leads to considerable confusion within various interested groups.

5.1.6 Laboratories

25. In Apulia the same five laboratories, as listed in the 2016 audit report, carry out official tests of samples, collected in the DA, for the presence of Xf. Four of these do the first level (screening) tests using the enzyme linked immunosorbent assay (ELISA). The laboratory of the National Research Council, Institute for Sustainable Plant Protection, Bari (CNR) deals with the validation of positive and doubtful results as well as quality control of the ELISA tests using real-time polymerase chain reaction (RT-PCR). The CNR also carries out subspecies identification with multi locus sequence typing (MLST). 26. Until December 2017 samples from the non-DA part of Apulia were analysed by the ELISA method and 1% of the samples were re-tested by RT-PCR by the CNR laboratory for quality control purposes. As the December 2017 amendment of the Decision requires molecular methods for samples taken outside the DA, in 2018 all of those samples were analysed with loop mediated isothermal amplification (LAMP) by the Mediterranean Agronomic Institute of Bari. 27. The Audit team noted that the testing regime, used in Apulia, is in line with provisions of Article 3(2) of the Decision as the methods used are listed in the Commission database of validated tests for the identification of Xf and its subspecies (https://ec.europa.eu/food/sites/food/files/plant/docs/ph_biosec_legis_emergency_comm-db-xylella- validated-tests.pdf). In addition, during the implementation of the tests, the laboratories follow the diagnostic protocol of the European and Mediterranean Plant Protection Organisation (EPPO) (PM 7/24(2)). 28. The CA stated that each ELISA laboratory works according to a detailed protocol, developed by the CNR. The laboratories use two types of commercial kits, which have a broad spectrum and are capable of detecting different subspecies of Xf. The CNR optimised the kits for olive plants, which are the main targets of the monitoring. The use of kits on host species other than olives resulted in rise of non-specific reactions considered as false positive results. Therefore a high number of the non-olive samples were re-tested with RT-PCR. As no difference was determined in the analytical sensitivity of the two kits, the laboratories’ choice is dictated by performance issues under their specific operating conditions (e.g. absence of background, speed of reaction development).

9 29. For verification and quality control purposes the laboratories using ELISA are obliged to send to the CNR the following plant samples, which are then re-tested:  each sample, which was tested positive by ELISA;  each sample, where the ELISA result was doubtful or non-determined;  5% of the daily samples tested negative by ELISA. This group must contain each sample taken from symptomatic plants, unless the share of symptomatic plants in the daily tests was above 5%. If there are more than 5% symptomatic samples, priority is given to non-olive hosts. In the case of non-symptomatic samples, priority is given to olive trees in risky areas and woody plant samples taken during the winter period. The CNR carries out molecular tests with leaves from the same plant material from which the first level laboratories have collected the required quantity of tissue for the ELISA test. The protocol used by the laboratories requires that ELISA and RT-PCR are carried out on the different portions of a leaf or petiole tissue from the same sample as it is technically impossible to use the same tissue extract in both diagnostic tests. 30. During the 2017 surveillance campaign, the CNR carried out quality control on 8,009 negative ELISA samples taken from the BZ and from the '20km zone'. Of those 309 (3.81%) tested positive. The audit team is of the view that the current false negative rate could be explained by:  The known significantly lower sensitivity of the ELISA method compared to the RT-PCR;  Performance issues of the laboratories using different kits and antibodies for the ELISA tests and  The use of different plant tissues of the same sample for the ELISA and RT-PCR tests, in the case of an uneven distribution of the bacterium in the sample. As regards the total number of samples from the BZ and '20km zone', analysed with ELISA during the 2017 monitoring campaign (see chapters 5.2, 5.3 and 5.4), this false negative rate means that many infected plants remained undetected. 31. In 2017-2018 the CNR carried out numerous MLST tests for the identification of the Xf subspecies, present in the DA. Samples from each new outbreak in the BZ and from each newly identified host were included in these tests supplemented by samples from numerous positive olive trees from different parts of the IZ. For the sequencing, DNA recovered from cultured isolates or directly from plant samples was used. The success rate of the MLST was practically 100% and in each case the presence of the subspecies pauca (sequence type (ST) 53) was confirmed. 32. The CNR also carried out new generation sequencing on isolates collected from different years. Each of those was identified as subspecies 'pauca' ST53 and the very minor differences in the generated genome data suggest that the bacterium was introduced quite recently into the area.

10 Conclusions on the organisational aspects of the plant health controls 33. In Apulia, regional legislation enables the implementation of the relevant provisions of the Decision. The competencies are clearly defined and distributed. 34. The lack of actions at national level to either grant a derogation or to speed-up the procedures required by the national legislation for the implementation of the eradication and containment measures in areas subject to national protection measures, as well as the related court appeals, has a serious impact on the proper implementation of the provisions of the Decision, in particular related to the immediate removal of positive plants and the clear-cut around them as appropriate. The delays diminish significantly the impact of the eradication and control measures and contribute to the rapid spread of the disease. 35. Although there is structured multichannel awareness raising activity in the Apulia Region, it does not have the intended effect towards non-professional olive growers, interest groups and the general public for counteracting the negative impact of inaccurate or misleading information related to Xf, which is currently present in the region. 36. The level of false-negative results, obtained by the ELISA tests raises serious concerns, as undetected infected plants significantly compromise the control measures and in particular the eradication in the buffer zone.

5.2 Surveys for the detection of Xylella fastidiosa in the demarcated area

Legal requirements Article 6(7) and Article 7(7) of the Decision.

Findings

37. The first annual survey in the current BZ and '20km zone' started in August 2016 and finished in May 2017. The 2017 annual campaign started in July 2017 and finished in May 2018. In both years the work started at the northern border of the BZ and progressed southwards. The survey was carried out by ARIF agents working in teams of two. The daily survey capacity ranged between 1,700-2,100 squares and 2,000- 2,500 plant samples. 38. ARIF worked according to a detailed protocol elaborated by CAs in Apulia. The audit team noted that the protocol is generally in line with the Commission guidelines for the survey of Xf in the Union territory, published in December 2015 (https://ec.europa.eu/food/sites/food/files/plant/docs/ph_biosec_legis_guidelines_xylella-survey.pdf) and, in certain aspects, goes beyond it. 39. The 2016 audit report describes in detail the survey method. In summary: In the BZ and '20km zone' the 100x100m grid approach was applied. The entire area of each grid square was checked visually to identify any host plant showing symptoms of potential infection. Samples were taken from each symptomatic plant and from the neighbouring plants as well. The RPS stated that during the 2016 campaign at least one plant sample was taken from each grid square where no symptoms were observed.

11 In the 2017 campaign in the BZ samples were taken only from some of those grid squares, where no symptomatic plants were detected. In the '20km zone' there were also grid squares, which were only visually checked without sampling. 40. The aim was to cover the entire physical territory of the two zones with the 100x100m grid squares. Only a limited number of squares with no access possibility (e.g. military fields) or without olive trees were omitted. 41. ARIF agents electronically recorded all relevant information about the surveys in the field with the help of a specific computer tablet application including the exact geographical position of sampled plants. After the daily field work, data were uploaded to a central database, operated by the regional agency 'Innovapuglia'. Plant samples were duly labelled and sealed before they were sent to the relevant laboratory (see chapter 5.1.6). The audit team noted that this approach ensures comprehensive data collection and full traceability of each individual plant after the laboratory tests 42. The audit team noted that  The method of grid based visual inspection and the associated sampling is in line with requirements of Article 3(1) of the Decision;  In both annual surveys, a considerable percentage of the grid squares in the BZ and '20km zone' were inspected during winter months. This period may be adequate for the visual inspection of olive trees and other evergreen species, but is not suitable for the detection of the key symptoms appearing on the leaves of deciduous and herbaceous plants;  This survey practice does not therefore take sufficiently into consideration the biology of the specified plants, although it is required by Article 3(1) of the Decision. Therefore the effectiveness of the visual inspections as a means of identifying symptomatic plants and suspected cases was compromised.  The report of the 2016 audit recommended to Italy to ensure that annual monitoring is carried out at times, which are appropriate for the detection of Xf in all specified plants in the BZ and in the '20km zone', as required by Articles 6(7) and 7(7) of the Decision (Recommendation No 1). The recommendation was not addressed.

5.2.1 Surveys in the buffer zone

43. The 2016 audit report describes in detail the 2016 annual survey in the BZ. The work was completed in December 2016. 51,712 grid squares were visually checked and 45,666 samples were taken. As in the entire BZ only 1,538 symptomatic hosts were identified, the majority of the samples were taken from asymptomatic hosts. Altogether 31 other specified plant species and genera were sampled. The highest numbers of samples were taken from Olea europea (85%), Asparagus spp. (3.2%), Nerium oleander (2.3%), Phyllirea spp. (1.8%), Myrtus communis (1.5%), Prunus dulcis (1.2%), Rosmarinus spp. (1.1%) and Cistus spp. (0.8%). One olive tree was tested positive (see table I.). 44. The 2017 grid based annual surveillance was completed in October 2017. 51,850 grid squares were visually checked and 13,247 samples were taken. Based on the results of the previous survey campaign, laboratory samples were not taken from each square, where symptomatic host plants were not identified. Each symptomatic plant was however sampled. Figures I. and II. in chapter 5.2.2 indicate the distribution of grid squares in the BZ in both sampling exercises, from which samples were taken.

12 45. During the 2017 surveys in the BZ, 20 specified plant species and genera were sampled. The majority of the samples (75%) were taken from Olea europea, followed by Prunus dulcis (7.4%), Phyllirea latifolia (4.4%), Asparagus acutifolius (3.4%), Rhamnus alaternus (3.1%), Nerium oleander (1.8%), Prunus avium (1.1%), Laurus nobilis (1.1%), Myrtus communis (0.8%) and Rosmarinus officinalis (0.7%). Nineteen olive trees were tested positive (see further details in table III. in chapter 5.3.2). Table I. The 2016 and 2017 annual surveys in the BZ No of No of squares Positive hosts Size of the square Annual survey samples inspected taken (olive trees)

2016 51,712 45,666 1 100m x 100m 2017 51,850 13,247 19 Source: RPS Apulia 46. In both years, visual inspection and sampling took place around the positive tested plants. In the 2017 campaign, 13 olive trees were found positive during the grid based exercise. During the monitoring in the 100m areas and beyond, 1,360 host and specified plants were sampled and another six olive trees tested positive (see further details in chapter 5.3.2). In some of the clear-cut areas in 2017, the owners requested derogation for certain 'monumental' olive trees. Each of those trees was sampled and tested negative. 47. After the amendment of the borders of the BZ in March 2018 (see chapter 5.1.2) the number of 100m x 100m grid squares increased by 7,773. In the period March-April 2018, some of those squares were inspected and samples were taken from symptomatic and non-symptomatic olive trees, all tested negative.

5.2.2 Surveys in the '20km zone'

48. As part of the 2016 campaign ARIF started surveying the '20km zone' in September 2016. First some high risk spots were checked while the systematic inspection of the grid squares from the northern border southwards started in October 2016. Although the inspection of the grids finished in February 2017, the surveillance of the 100m area around positive tested hosts lasted until May 2017. The total number of host plants, tested positive was 879; these were all of olive trees. 49. The 2017 annual surveillance in the '20km zone' started in September 2017. The grid based phase was completed by the end of March 2018, but the inspections in the 100m area of positive tested plants lasted until May 2018. The total number of positive plants, identified during the 2017 survey was 3,803 (see table II.). Figures I. and II. in chapter 5.2.2 indicate the geographical location of the positive tested plants. Table II. The 2016 and 2017 annual surveys in the '20km zone (including surveys around positive plants) No of No of squares Size of the square Annual survey samples Positive hosts inspected taken 2016 105,138 110,014 879 100m x 100m 2017 105,007 183,183 3,803 Source: MIPAAF, RPS Apulia

13 50. During the 2016 survey ARIF collected at least one sample from each square in the '20km zone' even if there were no symptomatic hosts. This practice was not followed during the 2017 survey, for the reasons mentioned in paragraph 39. 51. In both years, host plants surrounding the positives found during the grid based exercise were also sampled and tested. In the grid based phase of the 2017 campaign 756 plants tested positive, while checking the 100m area around those plants resulted in 3,047 additional positives, which were asymptomatic at the time of the grid based survey. These figures underline the importance of systematic checks around any positive detected during the grid based surveys, because there could be numerous asymptomatic trees present. Any delays in the felling of these trees could significantly compromise containment efforts (see details in tables IV and V. in chapter 5.4.2). 52. During the 2017 campaign, 28 specified plant species and genera were sampled in the '20km zone'. The majority of the samples (86.8%) were taken from Olea europea followed by Prunus dulcis (5.4%), Nerium oleander (1.4%), Laurus nobilis (0.6%), Myrtus communis (0.4%), Asparagus acutifolius (0.4%), Rosmarinus officialis (0.4%), Acacia saligna (0.2%), Phyllirea latifolia (0.2%) and Prunus avium (0.2%). 53. From the 3,803 plants, tested positive during the 2017 surveys 3,789 were Olea europea, eight Nerium oleander, two Acacia saligna, two Polygala myrtifolia, and two Prunus dulcis. 54. Figures I. and II. indicate the geographical location of the grid squares from which samples were taken and the geographical location of the plants which tested positive (see further details in chapter 5.4.1). The audit team noted that:  In 2016, the vast majority of the positives were found in the southern part of the '20km zone', and in particular in the municipalities Oria and Francavilla Fontana;  The 2017 figures show a massive increase of positives in the vicinity of the infected plants, detected in the previous year. This indicates that there is a very significant amount of inoculum in that part of the zone;  In 2017, many new positives were found in the central and northern part of the zone which could be explained by spread by human or natural means;  In the '20km zone', and in particular during the 2017 surveys, issues related to the survey time and the shortcomings of the ELISA test could have resulted in non- detection of a significant number of infected plants (see paragraphs 30 and 42).

14 Figure I. Results of the 2016 surveys in the BZ and '20 km zone'

Source: RPS Apulia, situation as of 09 May 2017 Legend: green area – grid squares from which samples were taken, red stars – positive plants, dark stars positives, already removed

Figure II. Results of the 2017 surveys in the BZ and '20 km zone'

Source: RPS Apulia (situation as of 18 May 2018) Legend: green area – grid squares from which samples were taken, red stars – positive plants, dark stars positives, already removed.

15 5.2.3 Surveys in the Infected Zone other than the '20km zone

55. The RPS informed the audit team that during the 2017 survey campaign, in the part of the IZ, other than the '20km zone', 153 squares of 100m x 100m were checked in the proximity of sites of plants with particular cultural, social or scientific value. Altogether 267 plant samples, mainly from olive trees were collected and eight tested positive. The audit team noted that this activity is in line with provisions of Article 7(7)(b) of the Decision. 56. No surveys were carried out in the proximity of nurseries, as there were no requests for the application of the derogation provided by Article 9(2) of the Decision. 57. The RPS stated that there are no comprehensive survey data or estimates available of the number of infected trees in the entire IZ or about the scale of economic impact of the disease. Various parties met by the audit team indicated that in the southern part of the IZ, the majority of the olive trees now show symptoms of different stages of decline. Many of these are dead or practically dead, producing only suckers.

5.2.4 Surveys in Apulia outside the demarcated area

58. For checking the possible presence of Xf outside the DA in the 2017 campaign, RPS applied a specific grid based approach. The area of the Region outside the DA was divided into squares about 1,000 ha. In each of those macro squares, 10 different squares of 100m x 100m were selected (i.e. 1% of the territory of the macro square was covered). Priority was given to service stations along the most important roads from the DA, areas alongside highways and railway lines as well as spots with high density of host (olive) plants. Host plants were visually checked and any symptomatic ones sampled. Samples from randomly selected asymptomatic hosts were also taken. A total of 7,734 micro squares were visually checked and 2,114 plant samples were taken. 59. The 2,114 samples were composed of 18 plant species. 70.9% of those were of Olea europaea, followed by Nerium oleander (12.1%), Prunus dulcis (5.2%), Laurus nobilis (4.4%), Rosmarinus officinalis (1.8%), Asparagus acutifolius (1.1%), Lavandula angustifolia (1.0%) and Polygala myrtifolia (1.0%). 60. In 2017 the outside DA samples were tested with ELISA and for quality control purposes 1% of the negatives were re-tested with real-time PCR. Since January 2018 the LAMP method is used. No positives were detected (see also chapter 5.1.7). 61. The audit team noted that the surveys outside the DA, including the laboratory tests, were in line with the relevant provisions of the Decision.

16 Conclusions on surveys for the detection of Xf 62. The survey method applied in the DA during the 2016 and 2017 annual campaigns was generally in line with the Decision. However, as a part of the visual inspections were carried out in periods not suitable for the detection of the key symptoms appearing on the leaves of deciduous and herbaceous hosts, many infected plants could remain undetected. 63. The 2016 and 2017 surveys finished in April and May of the following years leaving no time for the removal of all infected plants before the flight period of the vector started. The non-removed infected plants contributed to the rapid spread of the infection, in particular in the'20km zone'. 64. The 2017 surveys in Apulia outside the DA were carried out in line with the provisions of the Decision. Since January 2018 a more sensitive detection method is used as required by the Decision. 65. There were surveys in the IZ in areas other than the '20km zone' covering the proximity of certain sites with particular cultural, social or scientific value.

5.3 Eradication measures

Legal requirements Article 4 and Article 6 of the Decision.

Findings

5.3.1Establishment of a demarcated area

66. Following the detection of outbreaks in the BZ (see chapter 5.2.2.) the Regional Act DDS 109 of 19 March 2018 of the Agriculture, Rural Development and Environment Directorate amended its borders. The new border line is 10 km from the newly identified outbreaks. However, the borders of the IZ were not amended to incorporate all affected municipalities or land registry plots, although it is required by Article 4(2) third indent of the Decision. The report of the 2016 audit recommended to Italy to ensure that after an outbreak is detected in the BZ the delimitation of the BZ is immediately reviewed and changed accordingly, as required by Article 4(3) of the Decision (Recommendation No 3). This recommendation was not addressed. 67. The report of the 2016 audit also recommended Italy to erect road signs indicating the borders of the IZ and BZ as required by Article 6(8) of the Decision (Recommendation No 4). The RPS stated that no measures were implemented to that effect since the previous audit and therefore the recommendation was not addressed.

5.3.2Eradication measures in the Buffer Zone

68. The 2016 audit report describes in detail the eradication measures after an outbreak, detected in the BZ during the 2016 annual surveys. The sole infected olive tree detected in 2016 was felled nine days after the test results were confirmed and thereafter less than one month was necessary for the completion of the clear-cut. The audit report stated that the measures were in line with the provisions of the Decision.

17 69. Table III. contains detailed information about the measures related to the Xf outbreaks, which were detected in three of the municipalities in the BZ.

Table III. Measures in three municipalities in the BZ with Xf outbreaks

Grid based sampling Additional surveys Host plants Infected Felling/ Munici- removed in plants clear-cut pality Sampling Confirmed Posi- Sampling Plants Posi- the 100m removed (from-to) (from-to) test results tives (from-to) sampled tives vicinity of positives 04/09/17 18/09/17 18/09/17 2 297 1 41 / 12/10/17 19/10/17 06/12/17 07/09/17 18/09/17 19/09/17 08/02/18 10 672 5 14 154 24/10/17 21/10/17 09/11/17 17/05/18 Messapica 21/09/17 21/09/17 16/10/17 1 391 0 1 18 10/04/18 Ceglie 06/12/17 Total 13 1,360 6 14 213 Source: RPS Apulia 70. Figure III. indicates three neighbouring outbreak sites in the municipalities Ostuni and Cisternino, the delimitation of the 100m areas around the positive tested plants and the sampled plants within and outside the 100m circles

Figure III. Surveys related to Xf outbreaks in Ostuni and Cisternino

Source: RPS Legend: Green dots – negative tested plants, red stars – positive olive trees

71. Based on the information the RPS supplied the audit team noted that:  The grid based surveys were carried out in the territory of the three municipalities in September-October 2017. Samples from 13 olive trees tested positive. Some of the sites with positives were relatively close (less than 1km) to the border of the IZ, however others were at least 3-5 km away from the border of the IZ;  The confirmed laboratory test results (ELISA + RT-PCR) were available less than a month after the samples were taken;  Directly after the confirmation of the test results, surveys started in the vicinity of the outbreak sites. Specified plants in the 100m radius and also olive trees in the area beyond the 100m radius were sampled and tested (see figure III.). Altogether

18 1,360 samples were collected. At the end of 2017 six additional olive trees had tested positive;  Figure III. indicates that in some of the 100m areas established around the positives, the sampling and testing was not carried out fully in line with requirements of Article 6(3) of the Decision, as only a small number of samples were taken. On the other hand the numerous samples taken beyond the 100 m radius of the positives provided useful additional information for the delimitation of the outbreaks and the status of the entire BZ;  Directly after the confirmation of the positive test results, the RPS started the identification of the owners of host plants in the 100m areas. Some areas partly covered up to 10-20 land parcels and involved multiple owners in many cases. Despite such difficulties, all the host plant removal orders were issued before the flight period of the vector started;  In some of the outbreak sites, the removal of the infected olive trees and the clear- cut around them had started in the period February-May 2018. At the time of the audit 14 positive olive trees had been removed and 213 other host plants (mainly olive trees) had been felled in the 100m clear-cut areas around the positives. However, six positive olive trees detected in 2017 and numerous host plants (mainly olive trees) within the radius of 100m around the removed and remaining positives remained unfelled, which is not in line with requirements of Article 6(2) of the Decision which requires the immediate removal of plants known to be infected by Xf and any host plant regardless of their status in the 100m area;  'Monumental' olive trees were identified in some of the 100m areas around positives. In order to fulfil the requirements of Article 6(2)a of the Decision each of those trees were sampled and each tested negative. The plants were pruned heavily and were fenced with a 3m high protective (shading) net. The owners were advised to cut the grass under and around the trees and apply pest control. Figure IV. shows the method of physical protection of a monumental tree with netting on the sides but not on the top. The RPS stated that this protection method is based on the results of a Bari University study that in Apulia the vector does not fly higher than 3m. The audit team considers that the applied method does not ensure appropriate physical protection against the vector. Furthermore the Italian authorities did not notify the Commission about the protection method and agricultural practices. Therefore the protected trees do not fulfil requirements of Article 6(2a) of the Decision.  In summary only a part of the eradication measures, required by Article 6(2) of the Decision were implemented, in general with significant delays. At the time of the audit the completion time for the outstanding eradication work was unknown.

19 Figure IV. Protected monumental tree in a clear-cut areas in the BZ

Picture taken by the audit team

72. The audit team visited outbreak sites in the BZ where the eradication activity was initiated and noted that:  The felling of infected olive trees and the clear-cut in their 100m vicinity was carried out in line with the provisions of Articles 6(4) and 6(5) of the Decision;  Before the removal of the plants vector treatment was applied with authorised pesticides;  Olive trees and other ligneous plants were felled including the removal of roots to prevent the development of suckers;  The green parts (leaves, twigs) were destroyed by burning or chipping within the area;  The wood without leaves could be removed and used by the owner. Finally the land surface was levelled. The phytosanitary treatment and the removal method of host plants was fully in line with provisions of Article 6(4) and (5) of the Decision. Figure IV. shows the results of an already started clear-cut in Ostuni. Figure IV.Clear-cut, implemented partially in one outbreak site in the BZ

Picture taken by the audit team

20 73. The audit team noted that the following legal issues also contributed to the partial and delayed implementation of the eradication measures:  Some of the clear-cut zones include areas subject to national legislation on cultural heritage protection. Following the general rules (see paragraph 14 and 15) the regional administration had only just started the preparation of the environmental impact assessment for Soprintendenza and a speedy authorisation was not expected;  One of the owners lodged an appeal to TAR challenging the derogation from the regional landscape protection rules for the felling (see paragraph 7). The RPS stopped the felling of all olive trees subject to the derogation until the TAR reacts to the appeal.

Conclusions on the eradication measures 74. The lack of road signs means that the general public and the travellers are not sufficiently warned about the restriction on the movement of plants and about the area affected. 75. The significant delays and the non-completion of the eradication measures mean that infected and potentially infected host plants remain in the BZ during the 2018 flight period of the vector. This significantly compromises the protective function of the BZ and may necessitate more and severe eradication measures in the coming years.

5.4 Containment measures

Legal requirements Article 7 of the Decision.

Findings

5.4.1 Containment measures in the "20km zone"

5.4.1.1 Measures after the 2016 annual surveys

76. The 2016 audit report described the containment measures, which were carried out in the '20km zone' in 2016. In summary: When this zone was established by an amendment of the Decision in May 2016, there were six olive trees in the zone in the municipality of Oria, which tested positive in October 2015. All of these positives were in a grove in the close vicinity of the border of the '20km zone' to the other part of the IZ. The removal of the positive trees was blocked by a seizure order of the Prosecutor of Lecce, which banned any olive tree felling in the Region. The trees were only felled after the ban was lifted in the second half of 2016 or in 2017. RPS surveys in May-June 2016 identified a further 18 positive olive trees around the 2015 positives, which were removed in the last months of 2016 and in 2017. 77. Table IV. summarises the containment measures per municipality in the '20km zone' related to host plants tested positive as result of the 2016 annual survey. As it is described in chapter 5.2.2 the surveillance in the '20km zone', in particular around the positive tested host plants was completed with delays and some new positives were identified in May 2017, after the 2017 flight period of the vector started.

21 Table IV. Containment measures in the '20km zone' following the 2016 monitoring

Number of Sampling Felling order Felling Municipality positive (from to) (from to) (from to) plants 16/02/17 12/04/17 19/04/17 Brindisi 23 20/03/17 12/05/17 29/08/17 23/05/16 17/03/17 19/05/17 14 09/05/17 14/06/17 23/11/17 22/12/16 17/03/17 17/03/17 5 02/05/17 14/06/17 13/07/17 06/02/18 no Fragagnano 01/02/17 5 07/03/17 data 26/01/17 17/03/17 26/05/17 Francavilla Fontana 325 23/05/17 29/08/17 19/04/18 23/12/17 1 17/03/17 20/04/17 24/02/17 1 12/05/17 06/06/17 13/02/17 17/03/17 13/04/17 no 2 04/04/17 12/05/17 data Maruggio 02/03/17 1 22/05/17 13/06/17 15/02/17 03/04/17 27/04/17 Oria 492 09/05/17 08/11/17 19/04/18 03/04/17 2 12/04/17 15/04/17 04/04/17 21/12/16 18/07/17 Taranto 8 17/03/17 31/01/17 17/01/18 Total 879 Source: RPS Apulia 78. Over 90% of the positives which were identified during the 2016 campaign were in close vicinity of infected plants which were identified in 2015 and felled with significant delays. 79. The issuance of the felling orders started in March-April 2017 and in the case of municipalities with a limited number of positives it finished in the same month or in May and June 2017. However, in the two municipalities with the highest number of positives (Francavilla Fontana and Oria) it lasted until August and November 2017. The RPS stated that the land register did not provide up-to-date information and therefore the affected owners were identified and notified with significant delays. 80. The RPS stated that the removal of the 879 positive host plants, identified during the 2016 monitoring campaign was completed in April 2018. The audit team noted that:  In the municipalities with a limited number of positive hosts, the removal was finished in the period June-November 2017, usually one to three months after the issuance of the relevant RPS order;  In the two municipalities where 93% of the positives were identified the removal was finished in April 2018, on average five to eight month later than the issuance of the relevant RPS orders;  In some cases, however, the completion of the felling lasted up to one year after the positive status was identified.  The report of the 2016 audit recommended to Italy to ensure that at least all plants found to be infected by Xf in the'20km zone' are immediately removed as required

22 by Article 7(2) of the Decision (Recommendation No 5). This recommendation was not addressed. 81. The audit team noted that primarily due to the delays described above, the containment measures following the 2016 surveys were not in line with provisions of Article 7(2) of the Decision, which requires immediate removal of the host plants after the official identification of Xf. These delays contributed to the spread of the disease in the '20km zone'.

5.4.1.2 Measures after the 2017 annual surveys

82. Table V. summarises the containment measures per municipality in the '20km zone' related to the results of the 2017 annual surveys. As described in chapter 5.2.2, the surveillance in this zone and, in particular around positive tested host plants, was completed with significant delays. In the majority of the municipalities the last positives were confirmed in May 2018, within the flight period of the vector. Table V. Containment measures in the '20km zone' following the 2017 monitoring

Removed positive Grid based survey Survey in the 100m areas plants (08/06/18) Plants Posi- Munici- Confir- Confir- sampled tives pality Sampling Posi- Sampling mation Posi- Survey Num- mation total total % (from to) tives (from to) (from tives completed ber (from to) to) 27/11/17 12/01/17 27/02/18 19/03/18 Brindisi 143 25 no 2,479 168 1 0.6% 02/03/18 07/05/18 09/04/18 09/05/18 13/10/17 19/10/17 05/03/18 23/03/18 Carovigno 136 75 no 6,280 211 2 0.9% 21/12/17 07/02/18 09/03/18 14/05/18 Ceglie 20/09/17 18/09/17 06/03/18 26/03/08 135 103 no 15,016 238 89 37.4% Messapica no data no data no data no data 07/11/17 28/11/17 12/03/18 23/03/18 Fragagnano 1 1 yes 124 2 1 50.0% 21/12/17 11/12/17 14/03/18 27/03/18 Francavilla 25/10/17 16/11/17 05/03/18 13/03/18 190 948 no 30,760 1,138 249 21.9% Fontana 21/12/17 14/12/17 13/04/18 14/05/18 19/10/17 15/11/17 14/03/18 28/03/18 Grottaglie 1 0 yes 208 1 0 0.0% no data 24/11/17 16/03/18 30/03/18 18/10/17 07/11/17 28/02/18 17/04/18 Latiano 13 14 no 1,664 27 8 29.6% 13/03/18 30/03/18 06/04/18 11/05/18 19/10/17 11/12/17 22/03/18 03/04/18 Manduria 7 37 yes 182 44 1 2.3% 11/12/17 15/02/18 04/04/18 21/05/18 23/10/17 24/11/17 06/03/18 15/03/18 Maruggio 2 0 yes 797 2 2 100.0% 06/11/17 11/12/17 11/04/18 07/05/18 19/10/17 12/12/17 27/02/18 30/03/18 Oria 47 1,696 no 10,384 1,743 0 0.0% 21/12/17 07/02/18 13/04/18 11/05/18 22/09/17 13/10/17 05/03/18 15/03/18 Ostuni 13 11 no 4,054 24 8 33.3% 13/10/17 03/11/17 11/04/18 11/05/18

San 28/11/17 12/01/17no 30/10/17 Marzano di 1 no data 0 yes 76 1 1 100.0% no data data 13/03/18 S Giuseppe San 19/10/17 30/10/17 19/03/18 27/03/18 Michele 20 11 no 2,839 31 16 51.6% 12/03/18 27/03/18 16/04/18 14/05/18 Salentino San Vito 17/10/17 07/11/17 06/03/18 03/04/18 dei 20 36 no 3,661 56 9 16.1% 27/02/17 13/03/18 05/04/18 14/05/18 Normanni

23 Removed positive Grid based survey Survey in the 100m areas plants (08/06/18) Plants Posi- Munici- Confir- Confir- sampled tives pality Sampling Posi- Sampling mation Posi- Survey Num- mation total total % (from to) tives (from to) (from tives completed ber (from to) to) 24/10/17 21/11/17 09/03/18 09/04/18 Sava 8 9 no 2,137 17 8 47.1% 05/12/17 31/01/18 13/04/18 14/05/18 06/10/1/ 03/11/17 05/03/18 27/03/18 Taranto 10 6 yes 912 16 4 25.0% 09/11/17 11/12/17 13/03/18 27/03/18 Villa 02/10/17 03/11/17 07/03/18 26/03/18 9 75 no 2,590 84 9 10.7% Castelli 02/03/18 22/03/18 04/04/18 07/05/18 Total 756 3,040 84,163 3,796 408 10.7% Source: RPS Apulia

83. The audit team was informed that:  In the majority of the cases, the identification of the owners and the issuance of the felling orders for plants tested positive during the grid based surveys did not start until the surveillance in the 100m vicinity of the positives was completed and the confirmed test results were available;  In each municipality the identification of the owners started in the period March- May 2018. Although the majority of this work was completed, some information was still missing as of the time of the audit;  Until the end of May 2018, the RPS had issued 244 separate administrative decisions ordering the removal of 1,154 positive olive trees, i.e. 30.3% of the identified positives;  Until the end of May 2018 the removal of 408 positive tested hosts had been completed, which is 10.7% of the total;  The RPS stated that it intended to complete the identification of the owners and the issuance of the felling orders by the middle of July 2018. For this purpose the administrative staff of the headquarters was increased;  After having received the RPS plant removal order, the owners have 15 working days to complete the work;  The RPS stated that in each case, when the owner does not complete the felling in time the ARIF is commissioned to carry out the works immediately. 84. The audit team noted that:  Over 86% of the positives (more than 2,800 olive trees), identified during the 2017 campaign were found in Oria and Francavilla Fontana in the close vicinity of positive plants which were felled with significant delays after they were identified in the previous survey campaign;  Some of the positive tested host plants were removed after the flight period of the vector had commenced;  The RPS may be administratively capable to issue all the felling orders by mid-July 2018. However, it is very likely that the felling in numerous cases will be delayed by non-compliance and legal challenges by the owners;  In the event that there is widespread non-compliance by the owners, the ARIF, who is responsible for the removal, may not be able to deal with the task in a timely manner;  ARIF capacities will be divided between felling and surveillance, which could also cause significant delays in starting and completing the next (2018) survey campaign.

24 5.4.2 Containment measures in the IZ other than the "20km zone"

85. The audit team noted that in the IZ there were no production sites subject to the derogation of Article 9(2) of the Decision and therefore the application of provisions of Article 7(7)(a) was not necessary. 86. The audit team also noted that in the part of the IZ other than the '20 km zone' following the surveys carried out according to the provisions of Article 7(7)(b) of the Decision (see paragraph 55) not all of the olive trees which tested positive had been removed. This is not in line with provisions of Article 7(2) of the Decision.

Conclusions on the containment measures 87. Due to the delayed identification of infected plants and their owners after the 2016 and 2017 surveys, the majority of the felling orders were not issued in the '20km zone' before the flight period of the vector started in the following years. 88. Although all host plants which tested positive during the 2016 surveillance campaign were removed at the time of the audit, the excessive delays in felling the positive trees facilitated the continued spread of the pathogen during the 2017 flight period of the vector. 89. In the '20km zone' only a small fraction of the plants tested positive in the 2017 surveys had been removed before the start of the 2018 flight period of the vector. The completion of the felling, if completed at all, would take months. The large number of positives facilitated the rapid spread of the disease in the zone. Therefore the '20km zone', or at least a part of it, cannot sustain its intended function as a barrier against the spread of the disease. 90. The lack of removal of the positive tested host plants around sites subject to the provisions of Article 7(7)(b) of the Decision means that the plants with particular cultural, social or scientific value are not protected from being infected by Xf.

5.5 Appropriate agricultural practices

Legal requirements Article 7(6) of the Decision.

Findings

91. Regional orders require growers to carry out soil tillage and cut the undergrowth in and around olive groves in the period until after April in the entire territory of the DA. The relevant stakeholders are also obliged to cut the grass alongside roads, ditches etc. in the DA. The aim of these measures is to achieve a significant reduction of the juvenile vector population and with this mitigate the risk of the spread of Xf. 92. The Decree of 18 February 2018 of the Minister of Agriculture, Foodstuffs and Forest Policies orders olive growers in the DA to carry out chemical controls against the vector of Xf at least twice during the flight period with authorised pesticides following the principles of the integrated pest management. Treatments are obligatory in May and in August. The audit team was informed that this legal obligation was challenged by some organisations at the TAR.

25 93. CUFAA is responsible for controlling the implementation of the obligatory agricultural practices. Table VI. summarises the results of the inspections carried out in 2018. Table VI. Controls on the implementation of special agricultural practices in Apulia (2018) Non-conformity was Controls Province identified Number % Number % BARI 6 0.3% 6 100.0% BRINDISI 415 20.9% 53 12.8% LECCE 869 43.7% 132 15.2% TARANTO 699 35.1% 356 50.9% Average TOTAL 1,989 100.0% 547 27.5% Source: CUFAA 94. In 2018, by the time of the audit, CUFAA carried out 1,989 controls in the DA, including some inspections in Bari Province after the extension of the BZ (see chapter 5.3.1). Some areas were checked systematically while in other cases, a risk based, targeted approach was used. In the majority of the cases the soil tillage and grass cutting was checked as the first chemical vector control is mandatory only in May. The number of non-compliant cases in different provinces is indicated in Table VI. Each non-compliance case was sanctioned with a 1,000 euro flat rate penalty. 95. The audit team noted that:  The level of non-compliance was generally high and in particular in Taranto Province, where a large part of the BZ and '20km zone' is situated;  In particular in the IZ, the patchwork of compliant and non-compliant fields undermines the overall effectiveness and efficiency of the measures;

Conclusions on appropriate agricultural practices 96. The agricultural practices which were made obligatory by the Italian authorities in the DA for the management of Xf and its vectors, together with the removal of infected plants, would, if properly applied, assist significantly in the containment. However, the effectiveness is compromised by the partial implementation in the DA and by prolonged presence of infected trees on the ground.

5.6 Movement control of specified plants

Legal requirements Article 9 (movement ban, including derogations), Article 10 (traceability) and Article 11 (official checks) of the Decision.

Findings

5.6.1 Application of the derogation provided by Article 9(2) of the Decision

97. The RPS stated that nurseries in the DA currently do not market plants found to be susceptible to Xf subspecies pauca in Apulia. No requests had been received from

26 nurseries located in the DA for moving specified plants out of the DA or from the IZ to the BZ. 5.6.2 Official checks on movement of specified plants

98. A Regional Decision requires nurseries to establish an inventory of specified plants and to register and report their movement to professional operators. The RPS has developed a new IT tool to control movements of specified plants in the DA. Nurseries will be obliged to directly enter all incoming and outgoing movements into a central database. 99. CUFAA is responsible for the controls on the movement of specified plant within and from the DA. Table VII. and VIII. summarise the outcome of the inspections, which were carried out in 2017 and 2018. Table VII. Controls on the movement of specified plants in Apulia (2017)

Super- Non- Road Controls Non- Province Markets Nurseries markets, compliant controls total compliant shops % BARI 3 9 0 4 16 0 0.0% BAT 0 0 0 4 4 0 0.0% BRINDISI 5 3 43 71 122 8 6.6% FOGGIA 1 3 21 2 27 0 0.0% TARANTO 1 4 0 46 51 0 0.0% LECCE 23 11 60 32 126 9 7.1% TOTAL 33 30 124 159 346 17 4.9% Source: CUFAA Table VIII. Controls on the movement of specified plants in Apulia (2018) super- Non- Road Controls Non- Province Markets Nurseries markets, compliant controls total compliant shops % BARI 0 0 0 13 13 0 0.0% BAT 0 0 0 0 0 0 - BRINDISI 0 0 0 0 0 0 - FOGGIA 0 0 7 0 7 0 0.0% TARANTO 0 0 0 31 31 0 0.0% LECCE 0 0 10 0 10 2 20.0% TOTAL 0 0 17 44 61 2 3.3% Source: CUFAA

100. There were altogether 346 controls in 2017 and 61 in 2018. CUFAA stated that the 2018 checks would continue throughout the year. Non-compliance was identified in a relatively moderate share of the cases (17 in 2017 and 2 in 2018). The non-compliant cases were fined with a flat rate penalty of 1,000 euros. 101. The audit team noted that:  In 2017 the majority of the controls at places which may deal with specified plants were carried out in the IZ and in particular in the province of Lecce. There were many supermarket controls in Province Brindisi as well. Road controls

27 concentrated on the Province Lecce in the IZ and on the Province Taranto, a part of which belongs to the BZ and 20km zone;  In 2018 there were no controls in nurseries and in markets and checks were not carried out in two provinces of the region. The audit team considers that the number of inspection, and in particular the activities in 2018, do not provide for an appropriate level of controls. However, the applied penalties could be providing some deterrent. 102. There are no Xf related checks in ports and airports located in the DA despite the considerable number of travelers and volume of goods that leave the area via Brindisi Port and International Airport. Only posters are displayed about Xf in the passenger areas of the civil port and the airport. The RPS stated that it had not made arrangements with the relevant authorities or control bodies to inform passengers about the requirements or to carry out controls on outgoing traffic.

Conclusions on the movement control of specified plants 103. The currently applied movement control measures provide very limited guarantees that specified plants do not leave the DA including for other EU Member States.

6 OVERALL CONCLUSIONS

Although there is structured multichannel awareness raising activity in the Apulia Region, it does not have the intended effect towards non-professional olive growers, interest groups and the general public for counteracting the negative impact of inaccurate or misleading information related to Xf, which is currently present in the region. The rate of false negative results obtained by the ELISA tests raises serious concerns, as undetected infected plants in the DA significantly compromises the control measures, in particular the eradication in the buffer zone. The survey method applied in the DA during the 2016 and 2017 annual campaigns was generally in line with the Decision. However, as part of the visual inspections were carried out in periods not suitable for the detection of the key symptoms appearing on the leaves of deciduous and herbaceous host, many infected plants could remain undetected. Although all host plants which tested positive in the '20km zone' during the 2016 surveillance campaign had been removed at the time of the audit, the excessive delays in felling facilitated the continued spread of the pathogen during the 2017 flight period of the vector. Following the 2017 survey campaign, in the BZ, the eradication measures were only partially implemented and in the '20km zone' only 10.7% of the more than three thousand detected positive olive trees had been removed at the time of the audit. The lack of actions at national level to either grant a derogation or to speed up the procedures required by the national legislation for the implementation of the eradication and containment measures in areas subject to national protection measures cause significant delays in the removal of infected plants. Court appeals prevent the implementation of certain actions. Difficulties in the identification of the owners, and shortages in administrative capacities, contributed to the delays in the removal of infected plants. Unless urgent actions are taken, these issues are likely to continue as impeding

28 factors in the future. As a result of these shortcomings the protective function of the BZ is compromised and at least a part of the '20km zone' cannot sustain its intended function as a barrier against the spread of the disease. In particular, due to the high number of infected trees not removed until after the start of the 2018 flight period of the vector, a rapid northward spread of the disease is expected in 2018. The agricultural practices which were made obligatory by the Italian authorities in the DA for the management of Xf and its vectors would, if properly implemented, assist significantly in the containment. However, the efficiency is compromised by the partial implementation in the demarcated area. The currently applied movement control measures provide very limited guarantees that specified plants do not leave the DA, including for other EU Member States.

7 CLOSING MEETING

A closing meeting was held on 1 June 2018 at the headquarters of MIPAAF in Rome, during which the main findings and preliminary conclusions of the audit team were presented. The CA accepted the information provided by the audit team.

8 RECOMMENDATIONS

The NPPO of Italy is recommended to:

No. Recommendation 1. Ensure that annual monitoring is carried out, in the buffer zone and in the 20km part of the infected zone adjacent to the buffer zone, at times which are appropriate for the detection of Xylella fastidiosa in all specified plants as required by Articles 6(7) and 7(7) of Decision 2015/789/EU. The recommendation is based on conclusion No. 62. Associated finding No. 42. 2. Ensure that road signs are erected indicating the delimitation of the demarcated area as required by Article 6(8) of Decision 2015/789/EU. The recommendation is based on conclusion No. 74. Associated finding No. 67. 3. Ensure that after an outbreak is detected in the buffer zone eradication measures are implemented, in particular concerning the immediate removal of plants listed in Article 6(2) of Decision 2015/789/EU The recommendation is based on conclusions No. 34 and 75. Associated findings No. 11, 13, 14, 15, 16, 17, 18, 71 and 73. 4. Ensure that all plants found to be infected by Xylella fastidiosa in the 20km part of the infected zone adjacent to the buffer zone "20km zone" are immediately removed as required by Article 7(2) of Decision 2015/789/EU. The recommendation is based on conclusions No. 34, 87, 88 and 89. Associated findings No.11, 13, 14, 15, 17, 18, 76, 77, 78, 79, 80, 81, 82, 83

29 and 84. 5. Ensure that all plants which have been found infected by Xf based on the results of surveys, carried out in the proximity of the sites of plants with particular cultural, social or scientific value are removed immediately, as required by Article 7(2) of Decision 2015/789/EU. The recommendation is based on conclusion No. 90. Associated finding No. 86. 6. Ensure that increased official checks are carried out on specified plants being moved out of the demarcated area as required by Article 11 of Decision 2015/789/EU, including the establishment of controls on outgoing traffic at the international port and airport of Brindisi. The recommendation is based on conclusion No.103. Associated findings No. 101 and 102. 7. Identify the causes of the false negative results obtained with ELISA testing of plant samples taken from the demarcated area and introduce the necessary corrective actions to minimise false negative results. The recommendation is based on conclusion No. 36. Associated findings No. 29 and 30. 8. Consider to disseminate tailor-made information, in line with the provisions of Article 13a of Decision 2015/789/EU, in particular targeted to the general public and to non-professional olive growers, to counteract the negative impact of inaccurate and misleading information related to Xylella fastidiosa currently present. Based on conclusion No. 35. Associated finding No. 24.

The competent authority's response to the recommendations can be found at:

http://ec.europa.eu/food/audits-analysis/rep_details_en.cfm?rep_inspection_ref=2018-6485

30 ANNEX 1 – LEGAL REFERENCES

Legal Reference Official Journal Title Dir. 2000/29/EC OJ L 169, 10.7.2000, Council Directive 2000/29/EC of 8 May p. 1-112 2000 on protective measures against the introduction into the Community of organisms harmful to plants or plant products and against their spread within the Community

Dec. 2015/789/EU OJ L 125, 21.5.2015, Commission Implementing Decision (EU) p. 36–53 2015/789 of 18 May 2015 as regards measures to prevent the introduction into and the spread within the Union of Xylella fastidiosa (Wells et al.) ANNEX 2. RELEVANT INTERNATIONAL STANDARDS

International Title Standard

ISPM No. 9 International Standard on Phytosanitary Measures Publication No 9, Guidelines for pest eradication programmes, Food and Agriculture Organisation, Rome, Rome, Adopted 1998; published 2016, https://www.ippc.int/en/publications/611/

ISPM No. 14 International Standard on Phytosanitary Measures Publication No 14, The use of integrated measures in a systems approach for pest risk management, Food and Agriculture Organisation, Rome, Rome, Adopted 2002; published 2016, https://www.ippc.int/en/publications/607/

ISPM No. 31 International Standard on Phytosanitary Measures Publication No 31, Methodologies for sampling of consignments, Food and Agriculture Organisation, Rome, Adopted 2008; published 2016 https://www.ippc.int/en/publications/588/