Screening Potential Pests of Nordic Coniferous Forests Associated with Trade in Ornamental Plants

Bulletin OEPP/EPPO Bulletin (2020) 50 (2), 314–332 ISSN 0250-8052. DOI: 10.1111/epp.12667

Screening potential pests of Nordic coniferous forests associated with trade in ornamental plants

M. Marinova-Todorova1 ,N.Bjorklund€ 2 , J. Boberg3 , D. Flø4 , J. Tuomola1 , M. Wendell4 and S. Hannunen1 1Finnish Food Authority, Mustialankatu 3, Helsinki, FI-00790, Finland 2Department of Ecology, SLU Risk Assessment of Plant Pests, Swedish University of Agricultural Sciences, P.O. Box 7044, Uppsala, S-750 07, Sweden 3Department of Forest Mycology and Plant Pathology, SLU Risk Assessment of Plant Pests, Swedish University of Agricultural Sciences, P.O. Box 7026, Uppsala, S-750 07, Sweden; e-mail: [email protected] 4The Norwegian Scientiﬁc Committee for Food and Environment, P.O. Box 222, Skøyen, Oslo, 0213, Norway

Plant pests moved along with the trade in ornamental plants could pose a threat to forests. In this study plant pests potentially associated with this pathway were screened to identify pests that could pose a high risk to the coniferous forests of Finland, Sweden and Norway. Specifically, the aim was to find pests that potentially could fulfil the criteria to become regulated as quarantine pests. EPPO’s commodity study approach, which includes several screening steps, was used to identify the pests that are most likely to become significant pests of Picea abies or Pinus sylvestris. From an initial list of 1062 pests, 65 pests were identified and ranked using the FinnPRIO model, resulting in a top list of 14 pests, namely Chionaspis pinifoliae, Coleosporium asterum s.l., Cytospora kunzei, Dactylonectria macrodidyma, Gnathotrichus retusus, Heterobasidion irregulare, Lambdina fiscellaria, Orgyia leucostigma, Orthotomicus erosus, Pseudocoremia suavis, Tetropium gracilicorne, Toumeyella parvicornis, Truncatella hartigii and Xylosandrus germanus. The rankings of the pests, together with the collected information, can be used to prioritize pests and pathways for further assessment.

plants. For example, Kenis et al. (2007) and Santini et al. Introduction (2013) have shown that the majority of introductions of There is a general increasing global trade in products, and non-native insects and plant pathogens to Europe have been ornamental plants are no exception. Large amounts of associated with the international trade in living plants. Sim- plants and plant parts, such as cut trees and branches, are ilarly, almost 70% of the insects and pathogens that estab- brought into the Nordic countries for ornamental purposes lished in the United States between 1860 and 2006 most each year (Customs Finland, 2019; Statistics Sweden, 2019; likely entered on imported living plants (Liebhold et al., Statistics Norway, 2019). For example, almost all conifer- 2012). The likelihood of establishment of new non-native ous ornamentals used in Finland today originate outside the pests may also increase in the future in the Nordic countries country (Hannunen et al., 2014). During the last 10 years as a result of climate change. ornamental plants have been traded into Finland, Sweden The introduction of non-native plant pests through trade or Norway from more than 70 different countries (Customs is mitigated with plant health regulations, including lists of Finland, 2019; Statistics Sweden, 2019; Statistics Norway, quarantine pests and phytosanitary requirements for the 2019). These commodities may provide a pathway for non- international trade. New pests may be added to the lists if native pests with a potential to cause damage to the conif- they are assessed to fulfil the criteria of a quarantine pest erous forests of the region to which they are imported. according to the relevant International Standards for Phy- Pests of coniferous forests may be brought in with orna- tosanitary Measures (ISPMs) (FAO, 2007, 2013). mental plants not only with trade but also, for example, The aim of this study was to identify plant pests associ- when private individuals bring home plants from interna- ated with the trade in ornamental plants and plant parts that tional travel or when plants are brought in for research pur- could pose a high risk to the coniferous forests of Finland, poses. Sweden and Norway. Since the Nordic coniferous forests Invasive pests have caused extensive ecological and eco- are dominated by two species, Norway spruce (Picea abies) nomic impacts worldwide (Meyerson & Reaser, 2003; and Scots pine (Pinus sylvestris), the focus was placed on Hulme et al., 2008; Pejchar & Mooney, 2009) and they are these. Specifically, the objective was to identify pests that introduced into new areas especially via the trade in living potentially could fulfil the criteria to become regulated as

314 ª 2020 The Authors. EPPO Bulletin published by John Wiley & Sons Ltd on behalf of European and Mediterranean Plant Protection Organiza- tion, EPPO Bulletin 50, 314–332 This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes. Potential pests of coniferous forests 315 quarantine pests following the criteria set out in the Norwe- according to the Norwegian (Norwegian Ministry of gian (Norwegian Ministry of Agriculture & Food, 2017) Agriculture & Food, 2017) and EU plant health regula- and EU plant health regulations (EU, 2016). Another aim tions (EU, 2016). was to produce a database of all recorded pest species asso- (2) A database of pests associated with Picea spp. and ciated with Picea spp. and Pinus spp., and compile the Pinus spp. including information relevant for assessing information relevant for assessing whether the pests pose a the risk that they constitute. high risk to the coniferous forests in Finland, Sweden and Norway. The database can be used also in future assess- Screening and ranking process ments of pest risks to the Nordic coniferous forests. A stepwise approach as suggested by EPPO (2016) was used to identify the plant pests that constitute the highest Methodology risk for the Nordic coniferous forests and that may have the The methodology used for screening the pests associated potential to become regulated as quarantine pests according with ornamental plants was based on the EPPO Secre- to the Norwegian (Norwegian Ministry of Agriculture & tariat’s approach for commodity studies (EPPO, 2016). The Food, 2017) and EU plant health regulations (EU, 2016). methodology was adapted to meet the aims of the present The screening was divided into four steps and an additional study and performed as outlined below. The pests that were fifth step was used to rank the pests that received high rat- retained after the screening were ranked based on the prob- ings in the screening (Table 1). abilities of entry, establishment and spread, and the likely impact, using the FinnPRIO model and the hypervolume Step 1: Establishing a list of all pests of spruce (Picea spp.) approach (Heikkil€a et al., 2016; Yemshanov et al., 2017). and pine (Pinus spp.) A list of all recorded pests of Picea spp. and Pinus spp. was established using three major pest databases, i.e. the Scope EPPO Global Database (EPPO, 2018), the CABI Crop Pro- Area at risk tection Compendium (2018) and Pest Information Wiki The area at risk was Finland, Sweden and Norway. (2017). Pest species for which Picea spp. or Pinus spp., as well Focal plant species as Pinus sylvestris or Picea abies specifically, were listed The study focused on the identification of pest risks to the as hosts in the EPPO Global Database (EPPO, 2018) and two major native conifer forestry species in the area at risk, the CABI Crop Protection Compendium (2018) were namely Norway spruce (Picea abies) and Scots pine (Pinus extracted using the following key words: ‘Picea’, ‘Picea sylvestris). abies’, ‘Pinus’, ‘Pinus sylvestris’. The pest lists were retrieved from these databases in April 2018. The list of Commodities of interest pests associated with Pinus and Picea in Pest Information Commodities of interest included any species of ornamental Wiki (2017) was kindly provided by Bernhard Zelazny plants for planting, cut trees and branches intended to be from the International Society for Pest Information in used outdoors or indoors, regardless of whether they cur- December 2017. rently are traded to the area at risk. For plants for planting For each pest, information about the taxonomy and, when (i.e. plants intended to remain planted, to be planted or available, synonyms and EPPO Codes was obtained from replanted) all parts of the plant (e.g. leaves, branches, stem, the three databases. Since the information was collected bark and roots) and the growing medium used were consid- from three sources, the initial pest list contained some spe- ered as part of the commodity. For simplicity, the phrase cies more than once, with the same or different name. Such ‘the pathway ornamental plants’ is used in the rest of this duplicates were identified and the information merged by document. searching for records with the same scientific name, comparing the scientific name to the synonymous names of Type of pests considered other records and comparing the EPPO Codes (when avail- The plant pests considered in this study included insects, able) of the different pest records. arachnids, nematodes, fungi, chromists, bacteria, viruses and viroids. Step 2: Screening the pest list to identify potentially relevant species Origins considered The pest list was screened to only retain the pests that The origin considered was the entire world. could potentially pose a high risk and become regulated in the area at risk, i.e. Finland, Sweden and Norway. This was Output done by applying the following exclusion criteria: (1) A list of pests that may have the potential to fulfil the • First, since the focus of this study was on pests classified criteria to become regulated as quarantine pests as insects, arachnids, nematodes, fungi, chromists,

ª 2020 The Authors. EPPO Bulletin published by John Wiley & Sons Ltd on behalf of European and Mediterranean Plant Protection Organization, EPPO Bulletin 50, 314–332 316 M. Marinova-Todorova et al.

Table 1. An overview of the steps and outputs of the study

Step Aim Output

1 Establish a list of all pests of A list of pests, with scientific names, taxonomy and, when available, EPPO Codes Picea spp. and Pinus spp. 2 Screen the pest list to identify (1) A list of pests that need further consideration, with information on distribution, host plant potentially relevant species species, location of life stages on plant parts and the type of damage caused, and (2) a list of pests not considered further 3 Rate the pests against a number of A list of pests with ratings for each criterion, with justifications criteria 4 Select pests based on their ratings A list of selected pests that potentially can pose a significant risk to the Nordic coniferous forests 5 Rank the selected pests using the A list of pests ranked according to the risk they pose to the Nordic coniferous forests and a short FinnPRIO model and the description of the top ranked pests hypervolume approach

bacteria, viruses or viroids, other organism groups were Step 3: Rating the pests against a number of criteria excluded. To identify the pests that constitute the highest risk of those • Second, the pests that already were regulated (when the that were retained after Step 2, several rating criteria were study was conducted) were excluded, i.e. pests listed in used. The criteria, ratings and subratings used were based Annex I or II of Council Directive 2000/29/EC of the on the EPPO Secretariat’s approach for commodity studies European Union (European Council, 2000) and in the (EPPO, 2016) but adapted to the current study. In total six Norwegian Regulations of 1 December 2000 no. 1333 criteria were used: (Norwegian Ministry of Agriculture & Food, 2017). (A) Association with the pathway ornamental plants • Third, pest species known to be established in the area at (B) Host range risk were excluded. This was done based on the records (C) Climatic similarity in the Finnish, Swedish and Norwegian biodiversity infor- (D) Recorded impact mation species national databases (i.e. Laji.fi, Artpor- (E) Recorded interceptions talen.se, Dyntaxa.se, Artsdatabanken.no), information in (F) Known emerging pest the scientific literature and by consulting national experts. A detailed description of each criterion and their ratings are given in File S1 (see Supporting Information). In short, Finally, the retained pest species were divided into two criterion A was used to assess whether the pest could be groups: (1) pests that are present in Europe, but not present in carried on the pathway ornamental plants, considering the the area at risk, and (2) pests that are not present in Europe. plant parts that the pest’s different life stages are associated In the latter group pests were excluded if they were restricted with. Criterion B was used to rate the pests based on their to certain host plant genera (e.g. Abies, Cedrus, host range. This criterion also included a subrating that Chamaecyparis, Juniperus, Larix, Picea, Pinus, Pseudotsuga specified whether the pest species is known to be associated and Tsuga) whose import into EU or Norway is banned with the focal plant species in the area at risk, i.e. Picea (European Council, 2000; Norwegian Ministry of Agriculture abies and Pinus sylvestris. Criterion C was used to assess if & Food, 2017). This is because the pathway ornamental the pest is present in areas with climate similar to that in plants was considered to be closed for these pest species. the area at risk. This was done with the CLIMEX software The exclusion criteria were used one at a time. Once a and its ‘match regional climate’ algorithm (Kriticos et al., pest was excluded, further information was not collected. 2015). The analysis was carried out both in the present cli- For the remaining pests, further information about their dis- mate and using future climate scenarios for the time period tribution, host plants and pest characteristics (e.g. the loca- around 2050 (see File S1 for details of the analysis). Crite- tion of different life stages on the plant parts and the type rion D was used to rate the pests based on their recorded of damage they cause) was collected when readily avail- direct impact on coniferous species. Criteria E and F were able. used to identify pests that are known to move with trade There were some differences between the databases used and pests that have extended their distribution or are regarding which countries/regions were considered as a part becoming more damaging. of Europe. A precautionary approach was used where a pest When the rating was highly uncertain, the precautionary species was considered as present in Europe if it was principle was used, i.e. the highest potential rating was reported to be present in Europe in any of the databases. given. For pest species reported to be present in Russia, additional information about their distribution in the country was Step 4: Selecting pests based on their rating searched to determine whether the species were present in In this step, the pests constituting the highest risk were the European part of Russia or not. selected based on the ratings given in the previous step.

First, pests that have been recorded to cause mortality or impact, and risk. Hence, the scores are comparable with significant damages to coniferous plants, and that may be each other, but high scores do not necessarily mean that the carried with plants for planting, cut trees or branches were pest constitutes a high risk. selected. These were pests rated as high or medium for To provide an indication of whether some of the assessed their impact and assessed to be associated with the main pests may fulfil the ‘unacceptable impact’ criteria of quar- elements of the commodity. antine pests, four reference quarantine pests were also Then, from the list of pests present in Europe, only the assessed with FinnPRIO. The four reference pests were pests that are known to have Picea abies and/or Pinus Acleris variana, Cronartium harknessii, Lecanosticta sylvestris as hosts were retained. It was assumed that pests acicola and Pissodes strobi, which were all regulated as that are present in Europe and are a risk to Picea abies quarantine pests in the EU and Norway. It should, however, and/or Pinus sylvestris are likely to have been already be noted that Lecanosticta acicula has recently been re- recorded on these tree species considering their wide distri- evaluated and it is currently listed as a Union regulated bution in Europe. non-quarantine pest (European Commission, 2019), i.e. a From the list of pests not present in Europe, the selection non-quarantine pest whose presence in plants for planting was done based on the climatic similarity between the cur- affects the intended use of those plants with an economi- rent distribution area of the pest and the area at risk. Only cally unacceptable impact (FAO, 2019). Because the risk of the pests that occur in areas which were rated to have a the reference pests is already mitigated with the plant medium to very high climatic similarity with the area at health legislation, their entry and establishment scores are risk were retained. If the rating was medium, the presence not comparable with the scores of non-regulated pests. of the pest in climatically similar areas was verified by Therefore, only the magnitude of impact score was used to overlying the Koppen€ climate classification (Peel et al., compare the ranked pests with the reference pests. 2007) with presence observation points gathered from mul- The FinnPRIO assessments were done using the Finn- tiple databases (gbif.org, bison.usgs.gov, idigbio.org, inatu- PRIO graphical user interface (Marinova-Todorova et al., ralist.org, holos.berkeley.edu and ala.org.au). The ratings of 2019) with some modifications to the original assessment criteria E (Recorded interceptions) and F (Known emerging instructions by Heikkil€a et al. (2016). A detailed descrip- pests) were not used in the selection process, but the infor- tion of these modifications is presented in File S2 (see Sup- mation was used in the FinnPRIO assessments in Step 5. porting Information). The probability distribution of the scores for the likelihoods of entry, establishment and inva- Step 5: Ranking the selected pests using the FinnPRIO sion, and the magnitude of impacts (all ranging from 0 to model and the hypervolume approach 1) were simulated using R version 3.2.3 (R Core Team, The pests selected in the previous step were ranked using 2015) and R package ‘mc2d: Tools for Two-Dimensional the FinnPRIO model (Heikkil€a et al., 2016) and the hyper- Monte Carlo Simulations’ (Pouillot & Delignette-Muller, volume approach (Yemshanov et al., 2017). FinnPRIO is a 2010) with 1000 iterations. The lambda parameter of the pest ranking model that can be used to assess and compare PERT distribution was set to 1, implying a low confidence the risk that non-native plant pests pose to plant health. of the most likely estimate. Equal weight was given to eco- The model consists of multiple-choice questions with dif- nomic (50%) and environmental and social impacts (50%). ferent answer options yielding a different number of points. FinnPRIO expresses the assessment results as probability For each question the most likely answer option and the distributions that indicate the uncertainty of the assess- plausible minimum and maximum options are chosen based ments. The functional form of the distributions is not con- on a quick assessment of the available scientific evidence. sistent between the assessments and hence the distributions The given answer options are used to define a PERT proba- cannot be reliably described or ranked based on summary bility distribution that describes the uncertainty in the metrics, e.g. mean or median. To facilitate comparison of answer. The probability distributions of the final scores of the distributions, the hypervolume (HV) approach was used the likelihood of invasion, impact and risk are derived from to aggregate the distributions into a simple single-dimen- the question-specific PERT distributions using a Monte sional form that reveals the preference order relationship of Carlo simulation. The FinnPRIO model is described in the distributions (see Yemshanov et al. (2012, 2017) and detail in Heikkil€a et al. (2016). Tuomola et al. (2018) for details). In short, the hyperovol- In the current study FinnPRIO was used to separately ume approach establishes the relative order of the score dis- assess the pest’s likelihood of entry considering current tributions using a pairwise stochastic dominance rule and a official risk management measures, the likelihood of estab- hypervolume indicator. It first converts the probability dis- lishment (including spread), the likelihood of invasion (en- tributions into cumulative distribution functions, which are try 9 establishment), the magnitude of economic, then ordered using the pairwise stochastic dominance rule. environmental and social impacts, and the risk (likelihood This function establishes the ordinal rank order of the sub- of invasion 9 magnitude of impacts). The FinnPRIO model sets of the score distributions. Within a subset, none of the provides semiquantitative scores for the relative probabili- score distributions stochastically dominate other distribu- ties of entry, establishment and invasion, the magnitude of tions and hence the subset is treated as a single priority

ª 2020 The Authors. EPPO Bulletin published by John Wiley & Sons Ltd on behalf of European and Mediterranean Plant Protection Organization, EPPO Bulletin 50, 314–332 318 M. Marinova-Todorova et al. rank. The quantitative positions of the ranks, i.e. subsets of pests in Finland, Sweden and Norway, and 405 pests are score distributions, are estimated using the HV indicator already established there. From the remaining pests not pre- with a continuous measure from 0 to 1. sent in Europe, 216 were excluded because they only have The rankings with the pairwise stochastic dominance rule host plant species that cannot be imported into EU or Nor- and the HV indicator calculations were performed using a way according to the plant health regulations. Finally, 49 stand-alone program written in C++ that applies the hyper- pests were excluded because they were found not to be volume calculation algorithm from While et al. (2012). The pests of Picea spp. or Pinus spp. program was kindly provided by Denys Yemshanov from For the remaining 211 pests, information on their poten- Natural Resources Canada. The cumulative distribution tial association with the pathway, host range, distribution, functions were calculated from the score distributions at 60 impact and spread history was collected in a database and equal intervals and ordered using the first-order stochastic the pests were rated using the criteria in File S1. The rat- dominance rule to calculate the HV indicators. ings are presented in File S3. From these pests, according to the currently available information, 146 are present in Europe while 65 are not. About 80% of the pests consid- Additional analyses ered at this stage were insects or fungi (Table 2). The impact of climate change on the likelihood of estab- From the 211 rated pests, 65 were selected, based on their lishment of the rated pests in the area at risk was examined ratings, for the FinnPRIO assessments and the hypervolume using the CLIMEX analysis done in Step 3 (File S1). The ranking (Step 4, Fig. 1 and Table 3). These were pests that influence of using different pest species databases on the can potentially be associated with the main elements of the pests retained in each step was also analysed. commodity and have either high or medium recorded impact on conifers. In addition, the selected pests present in Europe are known to have Picea abies and/or Pinus sylvestris as Results hosts, while from the pests not present in Europe, only species that are present in areas with at least medium climatic Outcome of the screening similarity to the area at risk were selected. In total 1087 pest species records with unique scientific From the 65 ranked pest species, 38 were present in Eur- names were included in the initial list of pests of spruce ope while 27 were not (Table 3). The European countries (Picea spp.) and pine (Pinus spp.). After removing dupli- that had the highest number of the selected pests present cates (pests recorded in the databases with different syn- within their territories were Italy, France, Germany, the onyms), 1062 unique pest species records remained United Kingdom and Spain, with 22, 17, 17, 17 and 16 of (Fig. 1). Of these, 851 pests were not considered further the selected pests present, respectively (Fig. 2). The non- since they fulfilled at least one of the exclusion criteria European countries that had the highest number of the (File S3) (see Supporting Information). Out of the excluded selected pests present within their territories were the USA, pests 70 did not belong to the taxonomic groups considered Canada, China, Japan and Mexico with 38, 28, 21, 8 and 8 in this study, 111 pests are already regulated as quarantine pests, respectively.

Fig. 1 The outcome of the different steps of the screening. [Colour ﬁgure can be viewed at wileyonlinelibrary.com]

Table 2. The number of rated pests by pest type (Step 2) pine tortoise scale Toumeyella parvicornis and the fungal pathogen Coleosporium asterum s.l. Type of pest Number of species Based on the likelihood of invasion, the fungal pathogen Arachnida 1 Dactylonectria macrodidyma received the highest rank fol- Bacteria 6 lowed by the fungal pathogen Truncatella hartigii. The Chromista 9 third highest rank was much lower than the first two ranks Fungi 48 and consisted of two pests, the fungal pathogen Cytospora Insecta 119 kunzei and the yellows disease phytoplasma ‘Candidatus Nematoda 27 Phytoplasma asteris’. These pests were also in the highest Viruses and viroids 1 rank for likelihood of entry. It should be noted, however, All 211 that some studies indicate that Truncatella hartigii and Cytospora kunzei may already be present in Sweden and Table 3. The number of the 65 ranked pests that potentially can pose a Truncatella hartigii in Norway (Lagerberg, 1912; Jørstad, significant risk to the Nordic coniferous forests by pest type and 1936; Strid et al., 2014) but whether they are established presence in Europe (Step 3 and 4) needs to be verified. Based on the magnitude of impacts, the group with the Type of pest Present in Europe Not present in Europe All highest rank consisted of the fungal pathogen Arachnida 1 0 1 Heterobasidion irregulare, the hemlock looper Lambdina Bacteria 2 0 2 fiscellaria and the Mediterranean pine beetle Orthotomicus Chromista 2 0 2 erosus. Because of a low likelihood of invasion these three Fungi 15 6 21 pests obtained a relatively low rank for risk (Table 5). The Insecta 17 21 38 group with the second highest rank consisted of two insects, Nematoda 1 0 1 the finehorned spruce borer Tetropium gracilicorne and the Viruses and viroids 0 0 0 All 38 27 65 western pinewood stainer Gnathotrichus retusus. The pine needle scale Chionaspis pinifoliae obtained the third highest rank while the fourth rank contained a group of four insect Ninety per cent of the selected pests were insects or pests, namely the common forest looper Pseudocoremia fungi (Table 3). For each of the 65 selected pests, informa- suavis, the white-marked tussock moth Orgyia leucostigma, tion about their known distribution, host plants and a the alnus ambrosia beetle Xylosandrus germanus and the description of the impacts on conifers is given in File S3. pine tortoise scale Toumeyella parvicornis. The screening process showed that there were in general The mean impact scores of the FinnPRIO assessments were more known pests that constitute a risk to Pinus species highest for the two reference pests Cronartium harknessii and than Picea species, and more known pests that constitute a Pissodes strobi (Figs 3 and 4). These pests also received the risk to Pinus sylvestris than Picea abies (Table 4). For highest minimum and maximum scores. The scores of the example, 84% of the 1062 pests on the initial list were other two reference pests Acleris variana and Lecanosticta known to be pests on Pinus spp., while only 39% were acicola were lower than those of several of the ranked pests known to be pests on Picea spp. This was the trend in each (Fig. 3). The following 16 pests, ordered from highest to low- step of the screening. est rating, had higher mean impact scores than the reference pest with the lowest mean impact score (i.e. Lecanosticta acicola): Lambdina fiscellaria, Orthotomicus erosus, Results of the risk ranking Heterobasidion irregulare, Gnathotrichus retusus, Tetropium The hypervolume approach stratified the 65 ranked pests gracilicorne, Xylosandrus germanus, Orgyia leucostigma, into ordinal rank groups for each section separately Chionaspis pinifoliae, Toumeyella parvicornis, assessed with FinnPRIO. It created 14 ordinal rank groups Pseudocoremia suavis, Armillaria novae-zelandiae, Lygus for the likelihood of entry, 18 groups for the likelihood of lineolaris, Lygus Hesperus, Armillaria sinapina, Pityokteines establishment and spread, 19 groups for the likelihood of curvidens and Cytospora kunzei (Fig. 3). It should be noted, invasion, 20 groups for the magnitude of impacts and 19 however, that the impact assessments were limited to the groups for the risk (Table 5). potential damage of the pests on Picea abies and Pinus In terms of risk, the group with the highest rank consisted sylvestris in Finland, Sweden and Norway. The overall of the fungal pathogens Cytospora kunzei and Dactylonectria impact of the pests for the area at risk as well as for the EU macrodidyma (Table 5). The group with the second highest may be different should, for example, impacts on other hosts rank consisted of three pests, the white-marked tussock moth be included in the assessments. Orgyia leucostigma, the alnus ambrosia beetle Xylosandrus The ranked pests that were present in Europe generally germanus and the fungal pathogen Truncatella hartigii. The had higher likelihood of invasion scores than the pests not group with the third highest ordinal rank also consisted of present in Europe, while the magnitude of impact scores of three pests, the pine needle scale Chionaspis pinifoliae, the these groups were not clearly different (Fig. 4B).

ª 2020 The Authors. EPPO Bulletin published by John Wiley & Sons Ltd on behalf of European and Mediterranean Plant Protection Organization, EPPO Bulletin 50, 314–332 320 M. Marinova-Todorova et al.

Fig. 2 The number of pests, out of the 65 ranked pests present in different countries. [Colour ﬁgure can be viewed at wileyonlinelibrary.com]

Table 4. The number of known pests of species in the Pinus and/or Picea genera, and the number of pests that are known pests particularly on Pinus sylvestris and/or Picea abies

Step All Pinus spp. Picea spp. Pinus spp. and Picea spp. Pinus sylvestris Picea abies Pinus sylvestris and Picea abies

1 1062 887 (84%) 418 (39%) 244 (23%) 2 211 193 (91%) 77 (36%) 59 (28%) 60 (28%) 30 (14%) 14 (7%) 3 and 4 65 56 (86%) 41 (63%) 32 (49%) 32 (49%) 19 (29%) 11 (17%)

The proportion of the number of pests from all pests is in brackets.

opportunistic behaviour, the pathogen may already be estab- Description of top ranked pests lished in the area at risk, but not reported. Short descriptions of the 14 pests that were top ranked for Conclusion: The expected impact of this pathogen was risk and impact are given below (cf. Table 5). The main ranked relatively low, but it received the highest risk rank uncertainties that could be addressed in pest risk assess- of all assessed pests due to its very high likelihood of inva- ments and some other information that may be relevant sion. Further investigation is needed to conﬁrm whether the for risk management decisions are also provided (see File pathogen is already established in the area at risk. S3 for more information about the 65 pests that were ranked). Cytospora kunzei (risk rank 1, HV risk indicator 0.63). Cytospora kunzei is a fungal pathogen reported from The pest species ranked highest for risk North America, Asia, South Africa and Europe (Farr & Dactylonectria macrodidyma (risk rank 1, HV risk indicator Rossman, 2019). The fungus may already be established in 0.63). Dactylonectria macrodidyma is a fungal pathogen Sweden as it was found in decaying logs of Picea abies reported from North and South America, Australia, New and associated with bark beetles in two locations in Upp- Zealand and South Africa and from several countries in land (Strid et al., 2014). The pathogen is reported from dif- Europe (Farr & Rossman, 2019). The fungus causes dis- ferent conifer host species causing canker disease and eases in different hosts, e.g. black foot disease of Vitis spp. dieback of trees (Sinclair & Lyon, 2005). Picea abiesis (Halleen et al., 2004). In Lithuania, the fungus has been reported to be susceptible in the USA (Clement et al., found in seedlings of both Picea abies and Pinus sylvestris 2006). Pinus sylvestris is also reported as a host (Farr & in forest nurseries, clear cuts and farmlands (Menkis et al., Rossman, 2019), but the susceptibility is unclear. The 2006). The fungus has been isolated from both healthy- pathogen causes disease in trees stressed by, for example, looking roots and roots with disease symptoms and is sug- drought, but mortality of the affected trees is rare (Sinclair gested to be an opportunistic pathogen causing disease in & Lyon, 2005). Damage is mainly reported from ornamen- stressed seedlings (Menkis & Vasaitis, 2011; Menkis & tal trees (e.g. Christmas trees) and trees in windbreaks but Burokiene,_ 2012). Considering its wide global distribution, also from plantations (USDA, 1998, 2011a; Kavak, 2005; the association with seedlings in nurseries and its Natural Resources Canada, 2019a).

Table 5. The HV indicators of the pests assessed with FinnPRIO [Colour table can be viewed at wileyonlinelibrary.com]

Type of pest: A, arachnida; B, bacteria; C, chromista; F, fungi; I, insecta; N, nematoda. Top ranked pests are written in bold.

ª 2020 The Authors. EPPO Bulletin published by John Wiley & Sons Ltd on behalf of European and Mediterranean Plant Protection Organization, EPPO Bulletin 50, 314–332 322 M. Marinova-Todorova et al.

Fig. 3 The FinnPRIO scores for the magnitude of impact of the 65 ranked pests (ﬁlled circles) and the four reference pests (open circles). The dots and circles represent the means and the whiskers the minimums and maximums of the simulated probability distributions and hence indicate the uncertainty of the assessment. The pests are ordered from high to low impacts based on the means.

Fig. 4 FinnPRIO likelihood of invasion scores plotted against the magnitude of impact scores of the 65 ranked pests. The circles show the means and the whiskers show the minimums and the maximums of the probability distributions and hence indicate the uncertainty of the assessments. (A) The four thick horizontal lines represent the means for the four regulated reference pests (---, Cronartium harknessii; ÁÁÁ, Pissodes strobe; —, Acleris variana; —Á—, Lecanosticta acicola). (B) The ﬁlled circles represent the pests that are not present in Europe and the open circles represent the pests that are present in Europe.

Conclusion: This pathogen ended up in the highest risk Truncatella hartigii (risk rank 2, HV risk indicator rank based on a relatively high score for both invasion and 0.35). Truncatella hartigii is a fungal pathogen reported impact. Further investigation is needed to confirm whether from North America, Asia, South Africa and numerous the pathogen is already established in the area at risk. countries in Europe (Farr & Rossmann, 2019). The fungus has a very broad host range, including both conifers and Orgyia leucostigma (risk rank 2, HV risk indicator broadleaved tree species as well as cereals (Farr & Ross- 0.35). Orgyia leucostigma, white-marked tussock moth, has man, 2019). Both Picea abies and Pinus sylvestris have a distribution limited to North America, where it is native been recorded as hosts. The fungus has been isolated from (CABI, 2019a). There are, however, unconfirmed records of pine seeds and cones (Vujanovic et al., 2000), and is asso- the pest from England (Wilstermann & Schrader, 2018). ciated with stem girdling of seedlings in nurseries (Spauld- The pest is very polyphagous, and the list of its known ing, 1961). There are reports of the pathogen from hosts includes both trees and herbaceous plants (CABI nurseries in Norway and Sweden (Lagerblad, 1912; Jørstad, Plantwise Knowledge Bank, 2019a). Pinus strobus is one of 1936). There are also records from Finland, Norway and its main hosts, but it is primarily considered to be a pest of Sweden in Farr & Rossman (2019) citing sources not read- broadleaved trees (CABI Plantwise Knowledge Bank, ily available. Thus, the pathogen could already be estab- 2019a; Natural Resources Canada, 2019d). It may attack lished in the area at risk but that needs to be confirmed. conifers when the population is high and may cause severe Conclusion: Truncatella hartigii was ranked high due to damage in Christmas trees (Natural Resources Canada, the likelihood of invasion although its expected impact was 2019d). The pest has been a quarantine pest in Mexico ranked relatively low. Further investigation is needed to since 2018 (EPPO, 2019). According to an express Pest confirm whether the pathogen is established in the area at Risk Analysis (PRA) the phytosanitary risk of Orgyia risk. leucostigma for EU member states is high with high certainty (Wilstermann & Schrader, 2018). Xylosandrus germanus (risk rank 2, HV risk indicator Conclusion: Orgyia leucostigma received a relatively low 0.35). Xylosandrus germanus, black timber bark beetle, is rank for likelihood of invasion while the potential impact an ambrosia beetle native to Asia (CABI, 2019b). The bee- was ranked high. The assessment of the potential impact on tle has been introduced into North America and many coun- Pinus sylvestris was, however, highly uncertain. According tries in Europe (Bjorklund€ & Boberg, 2017; EPPO, 2019; to an express PRA done in 2018, the risk is high with high CABI, 2019b). In Sweden, the pest has been trapped twice certainty (other hosts than ornamental plants were also con- but it is not considered as established (Bjorklund€ & Boberg, sidered in that assessment). 2017). The beetle colonizes both broadleaved and conifer

ª 2020 The Authors. EPPO Bulletin published by John Wiley & Sons Ltd on behalf of European and Mediterranean Plant Protection Organization, EPPO Bulletin 50, 314–332 324 M. Marinova-Todorova et al. tree species, including Picea abies and Pinus sylvestris infect the needles and infection levels can be heavy. Dam- (CABI, 2019b). A rapid PRA was performed for Sweden in age, however, is usually limited to mainly defoliation and 2017 where it was concluded that Xylosandrus germanus stunted growth of small trees and Christmas trees (Sans- does not fulfil the criteria to become a protected zone quar- ford, 2015 and references therein). Several interceptions on antine pest in Sweden, perhaps due to limited possibilities cut flowers of Solidago sp. and Solidaster sp. have been to prevent natural spread from Denmark (Bjorklund€ & reported from the UK (Sansford, 2015). Coleosporium Boberg, 2017). asterum has been a quarantine pest in Mexico since 2018 Conclusion: A recent rapid PRA for Sweden concluded (EPPO, 2019). A PRA was performed for Coleosporium that Xylosandrus germanus does not fulfil the criteria to asterum in the UK in 2015 where statutory actions were become a protected zone quarantine pest in Sweden. not considered appropriate/justified (Sansford, 2015). Conclusion: The species delimitation is currently not Chionaspis pinifoliae (risk rank 3, HV risk indicator 0.31; clear. Based on the spread history, the likelihood of inva- impact rank 3, HV impact indicator 0.67). Chionaspis pini- sion was assessed as rather high but the impact on Pinus foliae, pine leaf scale, is an armoured scale probably native sylvestris in the area at risk was assessed to be lower than to North America, and also found in a few countries in that of many other ranked pests. In a PRA from 2015 for South America and Africa (CABI, 2019e). It is a pest of the UK, statutory actions against the pest were not consid- conifers with known hosts in the genera Pinus (main), ered necessary. Abies, Cedrus, Cupressus, Juniperus, Picea, Pseudotsuga, Taxus, Torreya and Tsuga (CABI, 2019e). Pinus sylvestris Toumeyella parvicornis (risk rank 3, HV risk indicator appears to be susceptible (Eliason & McCullough, 1997). 0.31; impact rank 4, HV impact indicator Damage seems to usually be limited to nurseries, Christmas 0.66). Toumeyella parvicornis, pine tortoise scale, is native tree plantation and ornamental trees (Eliason & McCul- in North America and has been introduced to several Carib- lough, 1997; Tooker & Hanks, 2000 (and references bean islands and Italy (Garonna et al., 2015; Malumphy & therein); Quesada & Sadof, 2017). The pest could be asso- Anderson, 2016). Its host range is limited to Pinus spp., ciated with ornamental plants (see, e.g. Green, 1930) and it and Pinus sylvestris is reported as one of the primary hosts has previously been introduced to new continents (CABI, (Clarke, 2013). The pest is reported to cause mortality of 2019e), but the import of plants for planting in the EU of seedlings, saplings and dieback of branches of Christmas most of the known host genera of the pest is banned from trees in North America, and in the Caribbean high mortality outside of Europe. has been observed (Malumphy et al., 2012; Clarke, 2013; Conclusion: The potential impact of Chionaspis Natural Resource Canada, 2019c). Due to, for example, a pinifoliae appears to be limited to nurseries and ornamental less favourable climate, similar high levels of damage are trees. The likelihood of invasion was assessed to be rela- not expected in the area at risk (Malumphy & Anderson, tively low but there is no import ban for two host genera of 2016). The pest is associated with seedlings and could the pest, i.e. Cupressus and Torreya (European Commis- thereby be associated with traded plants for planting but sion, 2019). import of Pinus spp. plants for planting from outside of Europe is banned. Coleosporium asterum s.l. (risk rank 3, HV risk indicator Conclusion: Toumeyella parvicornis is a known pest of 0.31). Coleosporium asterum, pine-aster rust, alternates Pinus sylvestris but since its impact in the area at risk is between hosts from Pinus and Asteraceae. The taxonomy expected to be limited to nurseries and ornamental trees, it and nomenclature of this species have recently been revised was ranked lower than the highest ranked pests. The likeli- (Beenken et al., 2017; McTaggart & Aime, 2018). hood of invasion was assessed as relatively low but orna- Coleosporium solidaginis has formerly been considered a mental Pinus plants from Italy are a potential pathway of synonym, but recent studies show that they are not con- entry. Further work could evaluate the need to regulate this specific (Beenken et al., 2017; McTaggart & Aime, 2018). pest as a regulated non-quarantine pest. Coleosporium solidaginis is found on Pinus spp. and Solidago spp., assumed to be native to North America, but Pest species ranked highest for impact has spread to Asia and Europe (Beenken et al., 2017; The following pests all received a high rank for potential McTaggart & Aime, 2018). Coleosporium asterum is impact but a relatively low invasion rank for the assessed instead found on Pinus spp. and Aster spp. (Beenken et al., pathway of introduction. 2017), is assumed to be native in Japan, but has also been reported from other countries in Asia (McTaggart & Aime, Heterobasidion irregulare (impact rank 1, HV impact indi- 2018). Due to the recent taxonomic separation of the two cator 0.96). Heterobasidion irregulare is a fungal pathogen species both their distribution and host range are uncertain causing root and butt rot. It is native to North America and and here the species were treated together as Coleosporium has been introduced into Italy where it is reported to cur- asterum s.l.. Both species have been found infecting Pinus rently have a restricted distribution (EPPO, 2019). The sylvestris (Farr & Rossman, 2019). On Pinus spp. the fungi main hosts belong to the Pinaceae and Cupressaceae,

ª 2020 The Authors. EPPO Bulletin published by John Wiley & Sons Ltd on behalf of European and Mediterranean Plant Protection Organization, EPPO Bulletin 50, 314–332 Potential pests of coniferous forests 325 especially species belonging to Pinus and Juniperus. Both beetle breeds in species belonging to the genus Pinus, Pinus sylvestris and Picea abies have been confirmed as including Pinus sylvestris (CABI, 2019d). It is normally hosts in inoculation studies (EPPO, 2015 and references regarded as a secondary pest infesting wood that recently therein). In 2015, a PRA was conducted for the EPPO died and stressed trees, but it has also been reported to region where the risk was assessed to be high with a mod- attack healthy trees following population build-up (CABI, erate uncertainty (EPPO, 2015). It was considered that the 2019d and references therein). The risk of this pest has pathogen could possibly establish as far north as the native been assessed for the USA (USDA Forest Service, 2018). species Heterobasidion annosum s.s. (62°N) and could add In the current study, entry to the area at risk via the path- to the high impact caused by it (EPPO, 2015). way ornamental plants was assessed to be very unlikely. Heterobasidion irregulare has a higher saprophytic ability However, entry through pathways other than plants for and a higher production of fruit bodies than Heterobasidion planting may be more likely since the pest has been inter- annosum s.s., and the two species have also been reported cepted, for example in G€avle harbour in 1988 on imported to commonly hybridize with unknown consequences wood from France (ArtDatabanken, 2019), and in CABI (EPPO, 2015 and references therein). The pathogen is not (2019d) bark, stems and wood packing material with bark reported to be associated with plants in nurseries and the are mentioned as a possible pathway whereas plants for likelihood of entry on plants for planting was assessed to planting is not. be low in the EPPO PRA. The assessment was, neverthe- Conclusion: The assessed potential magnitude of impact less, highly uncertain and the likelihood of entry would be was high but associated with a high uncertainty. Commodi- highest for larger plants (EPPO, 2015). The pathogen has ties other than ornamental plants are more likely pathways been a quarantine pest in Morocco since 2018 (EPPO, of entry. 2019). Conclusion: A PRA for the EPPO region was performed Tetropium gracilicorne (impact rank 2, HV impact indicator in 2015 and the risk was assessed to be high and the patho- 0.76). Tetropium gracilicorne, finehorned spruce borer, is gen is included in the EPPO A2 list. Commodities other a long-horned beetle found in the northern parts of Asia than ornamental plants are more likely pathways of entry and across Russia to Europe; from the Russian Far East to (EPPO, 2015). central Russia (EPPO, 2019). There is, however, an ongo- ing discussion on whether or not Tetropium gracilicorne is Lambdina fiscellaria (impact rank 1, HV impact indicator synonymous with Tetropium gabrieli since there are no 0.96). Lambdina fiscellaria, hemlock looper, is a polypha- reliable characteristics that can be used to distinguish the gous moth native to North America (CABI Plantwise species from each other (Danilevsky, 2019). Historically Knowledge Bank, 2019b; CABI, 2019c). The pest has not these species have been separated based on their different been reported from other parts of the world (CABI, 2019c). distribution ranges, but Tetropium gabrieli has recently The pest causes periodic outbreaks and is considered a seri- expanded its range in Europe to areas rather close to the ous defoliator in Canada (Natural Resources Canada, distribution range of Tetropium gracilicorne (it is now 2019b). Abies spp. and Tsuga spp. are the main hosts but established in Sweden and possibly also in Finland close during outbreaks other species, such as Picea spp., are also to the border of Russia (Kahanp€a€a, 2017)). Pinus sylvestris defoliated, but the susceptibility of Picea abies is not is listed as one of the preferred hosts of Tetropium known (Tuffen et al., 2019; CABI, 2019c). A rapid PRA gracilicorne, as well as other species of Pinus, Picea, for Ireland and Northern Ireland from 2019 states that the Abies and Larix (EPPO, 2002). A PRA was performed in pest poses a considerable risk to coniferous forests in the 2015 for the United Kingdom (Tuffen, 2015) and there is EPPO region, where the climate is suitable for establish- an older short PRA from EPPO (2002). The pest is mainly ment (Tuffen et al., 2019). The likelihood of entry for all considered a secondary pest of stressed trees often found pathways assessed (plants for planting, cut foliage, mosses together with other pests (Tuffen, 2015). Most reports of and lichens, and wood) was rated as very unlikely or unli- impact are on Larix spp. (Tuffen, 2015). Plants for plant- kely with varying uncertainty (Tuffen et al., 2019). ing are considered a potential pathway mainly if the com- Conclusion: The recent PRA performed for Ireland and modity consists of larger plants of conifers (EPPO, 2005). Northern Ireland indicates that the pest poses a considerable The beetle has been intercepted on wood (Tuffen, 2015) risk for coniferous forests. The potential impact was ranked and entry through wood commodities may be more likely the highest, but the potential impact on Picea abies is (EPPO, 2005). highly uncertain since it has not been confirmed as a host. Conclusion: It is not clear if Tetropium gracilicorne is the same species as the already established Tetropium Orthotomicus erosus (impact rank 1, HV impact indicator gabrieli. The PRA from 2015 assessed the potential impact 0.96). Orthotomicus erosus, Mediterranean pine beetle, is for the UK as small. The potential magnitude of impact on found in Europe, particularly in the southern parts, in Asia Pinus sylvestris assessed here was highly uncertain. Wood and North Africa, and as an introduced pest in Fiji, South commodities may be a more likely pathway of entry than Africa, Swaziland and the USA (CABI, 2019d). The bark the pathway ornamental plants.

ª 2020 The Authors. EPPO Bulletin published by John Wiley & Sons Ltd on behalf of European and Mediterranean Plant Protection Organization, EPPO Bulletin 50, 314–332 326 M. Marinova-Todorova et al.

Fig. 5 Climatic similarity at country/state level for (A) present and (B) future climate. [Colour ﬁgure can be viewed at wileyonlinelibrary.com]

Gnathotrichus retusus (impact rank 2, HV impact indicator 0.76). Gnathotrichus retusus, western pinewood stainer, is an ambrosia beetle present in western North America, from Canada through the USA to Mexico (Atkinson, 2019). Both deciduous and conifer tree species are reported as hosts, including both Pinus spp. and Picea spp. (Atkinson, 2019). The pest colonizes and excavates galleries in recently cut logs, vectors blue stain fungi and is regarded as an economically important pest of stored timber in western North America (Liu & McLean, 1993; Deglow & Borden, 1998; Hollingsworth, 2019). The pest is not expected to attack living trees. The likelihood of entry to the area at risk from the USA through the pathway ornamental plants was here assessed as very unlikely. Fig. 6 Area-proportional Venn diagram of the overlap of pest species in The pest has been intercepted in Australia and New Zeal- the databases. [Colour ﬁgure can be viewed at wileyonlinelibrary.com] and on wood commodities and packaging material from the USA (USDA, 2011b) and entry through these path- Conclusion: The impact is expected to be limited to ways is considered more likely than entry through the effects on timber quality during storage. Other pathways pathway ornamental plants. than ornamental plants are more likely.

Fig. 7 The proportion of pest species included in the different databases remaining after the different steps in the screening procedure. [Colour ﬁgure can be viewed at wileyonlinelibrary.com]

Pseudocoremia suavis (impact rank 4, HV impact indicator were higher for the future climate in 35 countries and 30 0.66). Pseudocoremia suavis, common forest looper, is a regions (of Russia, Canada, the USA and China), and lower moth native to New Zealand (Berndt et al., 2004). It has only in 3 countries and 10 regions (Fig. 5). Moreover, more also been introduced into the UK (James, 2019). There are than 30% of the rated 211 pests and more than 15% of the also sporadic reports from the USA but whether or not the 65 ranked pests got higher ratings in the future climate than pest is established needs to be confirmed (iNaturalist, in the present climate, while none of the pests got a lower 2019). The pest is polyphagous and can feed on and defoli- rating in the future climate. ate both broadleaved and conifer tree species (Alma, 1977; Berndt et al., 2004). Pinus sylvestris is recorded as a suit- Exploration of the used pest databases able host for the pest (Dugdale, 1958). In New Zealand, it As expected, there was an overlap of pest species included is not considered a major pest of native trees, but has in the three pest databases and there was a large difference caused outbreaks in exotic conifer forests, e.g on Pinus between the number of pests obtained from each database radiata (Berndt et al., 2004 and references therein). It is (Fig. 6). In total 1062 pests were initially included in the thought that these outbreaks were associated with hosts current study. The database Pest Information Wiki (2017) stressed by, for example, drought and fungal disease, and contained 759 of these pests, the CABI Crop Protection they appear to have been short lived (Alma, 1977). The Compendium (2018) contained 581 of these pests and the moth has already spread to Europe (UK) and could be asso- EPPO Global Database1 (EPPO, 2018) contained informa- ciated with plants for planting. tion that Picea or Pinus was a host for only 106 of these Conclusion: The impact assessment was highly uncertain. pests (Fig. 6). Thus, a strikingly large proportion of the The likelihood of invasion was assessed as relatively low, pests was only found in one of the databases. but the pest has been introduced to the UK. Interestingly, there was no indication of any differences between the characteristics of the pests included in the different databases, i.e. the proportion of pests remaining after Additional analyses each step in our screening was similar in all three databases Comparing present and future climate (Fig. 7). There were no indications that stricter require- The CLIMEX analysis based on the present climate, using ments had been used for defining a species as a pest in the a 30-arc minute spatial resolution, showed that 39% of the databases which contained fewer pests. On the contrary, the world’s terrestrial area has a medium to very high similar- database from which most pests were obtained was the one ity with the climate in Finland, Sweden or Norway (Com- with the highest proportion of pests classified to have a posite Match Index values ≥0.7). The analysis of the future high recorded impact, i.e. 44% of the pests from the Pest climate scenarios for the time period around 2050 showed that this was the case for 36% of the area. However, when 1Note from the Editor: The EPPO Global Database (EPPO GD) con- the 30-arc minute spatial resolution analyses were con- tains basic information for 785 out of the 1062 pests considered. We verted into a country, or smaller region, level climatic simi- remind readers that the focus of EPPO GD is on regulated pests and does not intend to register all host plants but to focus on the most larity ranks, the situation changed. The similarity ranks important hosts.

ª 2020 The Authors. EPPO Bulletin published by John Wiley & Sons Ltd on behalf of European and Mediterranean Plant Protection Organization, EPPO Bulletin 50, 314–332 328 M. Marinova-Todorova et al.

Information Wiki, 26% from CABI CPC and 28% from the information on the biology and the ecology of the pests and EPPO Global Database. Consequently, the benefit of using other information that was initially used to assess the pests several databases was stronger than expected, i.e. 41 out of should also be taken into account. Such information was the 65 ranked pests that remained after the screening proce- summarized for the 14 top ranked pests in section 3.3. dure were only found in one database. Furthermore, three For some of the 65 ranked pests, relevant PRAs that out of the eight pests that received the highest risk ranks in could be used to guide risk management decisions already the FinnPRIO assessments were only included in one data- exist. Among the top ranked pests, PRAs for the EPPO base. region have been performed for Heterobasidion irregulare There was no indication of any differences between the (EPPO, 2015) and for Tetropium gracilicorne (EPPO, databases with regard to the proportion of different types of 2002). In addition, PRAs are available for Lambdina pests. In all three databases more than half of the pests fiscellaria for Ireland and Northern Ireland (Tuffen et al., were insects and approximately a quarter were fungi. Fur- 2019), Coleosporium asterum s.l. and Tetropium thermore, the screening procedure did not change the pro- gracilicorne for the UK (Tuffen, 2015; Sansford, 2015), a portions of the different types of pests retained. quick PRA for Xylosandrus germanus for Sweden (Bjork-€ lund & Boberg, 2017) as well as an express PRA for Orgyia leucostigma for the EU (Wilstermann & Schrader, Discussion 2018). The field of pest risk analysis has been criticized for being Comparison of the FinnPRIO impact assessments of the reactive rather than proactive (Brasier, 2008). The focus 65 ranked pests with the four reference pests indicated that tends to be on pests that have already caused damage out- the expected impact of some of these pests is in the same side of their native region. The current study is an attempt range as that of the quarantine reference pests. These pests to proactively identify all pests, including those that have are thus especially relevant for further investigations con- not yet established outside their native region, which could sidering their potential to cause damage to the Nordic pose a risk to the health of the coniferous forests of Fin- coniferous forests. Some of the pests that ranked high for land, Sweden and Norway. There are many trade require- expected impact were ranked relatively low for the likeli- ments and import bans of living plants in the plant health hood of invasion and thus did not get a high risk rank. One legislation that protect the coniferous forests of the Nordic of the main reasons for the low likelihood of invasion rank countries from new pest incursions. Nevertheless, our study for many of these pests was their low likelihood of associa- revealed many pests of Norway spruce (Picea abies) and tion with ornamental plants. However, for several of these Scots pine (Pinus sylvestris) that potentially could be intro- pests, such as Orthotomicus erosus and Gnathotrichus duced into the area at risk, i.e. Finland, Sweden and Nor- retusus, other pathways than ornamental plants may be way, via international trade in ornamental plants. more likely and might deserve further assessment given the Most of the pests that were identified to potentially con- pests’ high expected impact on the focal tree species. It stitute a significant risk to the Nordic coniferous forests are should, however, be noted that identification of other possi- present in Europe. This is partly a result of a high likeli- ble pathways was not done for all the assessed pests as it hood of introduction due to the free movement of most was not in the scope of this project. ornamental plants in the EU’s internal market. Because The assessment of the impacts was limited to the impacts many of these pests are widely established in Europe, they on Pinus sylvestris and Picea abies. However, some of the are unlikely to become regulated as Union quarantine pests identified pests are very polyphagous and although they in the EU. However, whether they fulfil the criteria to be were ranked low here, they could pose a serious risk to regulated as quarantine pests in Norway and/or as protected some other host plants present in the area at risk. zone quarantine pests in Finland and Sweden needs to be There are indications that some of the identified pest spe- assessed. The study also revealed several pests that are not cies may already be present in Finland, Sweden or Norway present in Europe but could potentially be introduced via but due to lack of reliable information they were considered the trade in ornamental plants. The sufficiency of the cur- not established in the area at risk. This was the case for rent phytosanitary requirements for preventing the introduc- three fungal species, Cytospora kunzei, Dactylonectria tion of these pests and the need for additional requirements macrodidyma and Truncatella hartigii, which were among is not known. Further studies, e.g. full PRAs, may be tar- the 14 top ranked pests. Further investigations are needed geted to some of the identified pests or to some of the host to confirm whether these pests are already established in plant commodities of these pests. the area at risk.

The ranked pests General pest patterns The hypervolume approach was used to rank the pests The geographic distribution of the pests should be consid- based on the FinnPRIO scores, but risk management priori- ered when planning further work with the identiﬁed pests. tization should not be based solely on the rankings. The The 65 ranked pests were not evenly distributed around the

ª 2020 The Authors. EPPO Bulletin published by John Wiley & Sons Ltd on behalf of European and Mediterranean Plant Protection Organization, EPPO Bulletin 50, 314–332 Potential pests of coniferous forests 329 world but stratified into certain countries. For example, trade in ornamental plants. For Chionaspis pinifoliae, 58% and 43% of these pests are present in the USA and Pseudocoremia suavis and Toumeyella parvicornis the next Canada, respectively, while only 22% of them are present step should be to further investigate their likelihood of within the countries of Africa. Presumably, these differ- introduction since those assessments were highly uncertain. ences are at least partly related to the distribution of the species in Pinus and Picea genera. Of the European coun- Acknowledgements tries, the highest number of the ranked pests (22) is found in Italy, which accounts for almost 60% of all the ranked The authors gratefully acknowledge the discussions with pests that are present in Europe. Melanie Tuffen about the project dealing with threats to The climatic similarity analysis indicates that the climate Sitka spruce in Ireland, the sharing of data from that project in the Nordic countries will become more suitable in the by the Agriculture and Food Development Authority (Tea- future for many of the pests that are still absent from this gasc) in Ireland, Bernhard Zelazny (International Society region. For many areas where the pests are currently pre- for Pest Information) for retrieving the list of pests from sent, the climatic similarity ratings were higher for the Pest Information Wiki, Denys Yemshanov (Natural future climate than for the present climate. Some of the Resources Canada) for providing the program to calculate pests got higher ratings for the future climate than for the the hypervolume indicators and the following experts for present climate, while none of the pests got a lower rating providing information regarding the presence of specific for the future climate. However, because the assessments pests in the area at risk: Asko Hannukkala (University of were based only on presence data of the pests at a high Helsinki and Natural Resources Institute Finland), Jarkko spatial resolution, they are highly uncertain. A more certain Hantula and Antti Pouttu (Natural Resources Institute Fin- estimate on the likelihood of establishment would require land), Pertti Salo (University of Helsinki), Torstein either information on the precise distribution of the pests Kvamme (NIBIO), Ylva Strid (Uppsala University), Ake within the countries or an analysis of the pests’ response to Lindelow,€ Martin Schroeder, Ida Karlsson and Ramesh various climatic variables. Vetukuri (SLU). Several pest databases were used to create the initial list that aimed to contain all known pests of Picea spp. and Selection et classement d’organismes associes Pinus spp. The benefit of using several databases was stron- au commerce de plantes ornementales ger than expected since 41 of the 65 ranked pests were only potentiellement nuisibles aux fore^ts nordiques found in one of the three used databases. This is notewor- de coniferes thy since that there was no indication of any difference between the types of pests that were included in the differ- Les organismes nuisibles aux vegetaux transportes via le ent databases. Thus, our study indicates that, when possible, commerce de plantes ornementales pourraient egalement several databases should be used in studies like this one. constituer une menace pour les forêts. Dans cette etude, les organismes nuisibles aux vegetaux potentiellement associes a cette filiere ont ete passes au crible afin d’identifier ceux Future outlook qui pourraient representer un risque eleve pour les forêts de In this study 65 pests that could potentially become signifi- coniferes de Finlande, de Suede et de Norvege. L’objectif cant pests of Picea abies or Pinus sylvestris in the Nordic etait plus precisement de trouver des organismes nuisibles countries were identified. These pests were ranked with the remplissant potentiellement les criteres pour être FinnPRIO model, and the 14 pests ranked highest for risk reglementes en tant qu’organismes de quarantaine. and/or impact were described in more detail. It is, however, L’approche developpee dans l’etude sur les marchandises apparent that factors other than these ranks should be con- de l’OEPP, qui comprend plusieurs etapes de selection, a sidered when deciding what should be done next. For ete utilisee pour identifier les organismes nuisibles qui sont example, PRAs are already available for several of the top les plus susceptibles de devenir importants sur Picea abies ranked pests, namely Coleosporium asterum s.l., ou de Pinus sylvestris. A partir d’une liste initiale de 1062 Heterobasion irregulare, Lambdina fiscellaria, Orgyia organismes nuisibles, 65 organismes ont eteselectionnes et leucostigma, Tetropium gracilicorne and Xylosandrus classes a l’aide du modele FinnPRIO, ce qui a abouti a une germanus. For these pests, the next step should be evaluat- liste de 14 principaux organismes nuisibles, a savoir ing if new PRAs are needed. For some pests, namely Chionaspis pinifoliae, Coleosporium asterum s.l, Cytospora Cytospora kunzei, Dactylonectria macrodidyma and kunzei, Dactylonectria macrodidyma, Gnathotrichus Truncatella hartigii, further investigation is needed to con- retusus, Heterobasidion irregulare, Lambdina fiscellaria, firm whether or not they are already established in the area Orgyia leucostigma, Orthotomicus erosus, Pseudocoremia at risk. The likelihood of invasion of Gnathotrichus retusus suavis, Tetropium gracilicorne, Toumeyella parvicornis, and Orthotomicus erosus via other pathways, such as wood, Truncatella hartigii et Xylosandrus germanus. Les might deserve attention since they were assessed to have classements des organismes nuisibles, ainsi que les high impact, albeit a low likelihood of invasion via the informations recueillies, peuvent être utilises pour

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ª 2020 The Authors. EPPO Bulletin published by John Wiley & Sons Ltd on behalf of European and Mediterranean Plant Protection Organization, EPPO Bulletin 50, 314–332