Risk assessments for pathways of IAS - Literature review

TSSR-2019-02

This note has been drafted by a team of experts under the supervision of IUCN within the framework of the contract No 07.0202/2016/739524/SER/ENV.D.2 “Technical and Scientific support in relation to the Implementation of Regulation 1143/2014 on Invasive Alien Species”. The information and views set out in this note do not necessarily reflect the official opinion of the Commission, or IUCN. The Commission does not guarantee the accuracy of the data included in this note. Neither the Commission nor any person acting on the Commission’s behalf may be held responsible for the use which may be made of the information contained therein. Reproduction is authorised provided the source is acknowledged.

This document shall be cited as:

IUCN. 2019. Risk assessments for pathways of IAS – literature review. Technical note prepared by IUCN for the European Commission.

Date of completion: 07/03/2018

Comments which could support improvement of this document are welcome. Please send your comments by e-mail to ENV-IAS@ec.europa.eu.

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Contents

Introduction..........................................................................................................................................3

The provisions of the Regulation (EU) No 1143/2014.......................................................................3

Main elements to consider in pathway analysis and prioritisation...................................................5

Main works supporting the development of methodologies for pathway analysis and prioritisation. .8

Examples of analysis made at the European level...........................................................................11

Examples of recent analysis made in Europe at the country/region level.......................................11

Pathway analysis of alien species in freshwater environments.......................................................13

Pathway analysis of alien species in marine environments.............................................................15

Other examples of pathway analysis...............................................................................................16

Pest Risk Analysis and Pathway Risk Analysis in the IPPC contest.......................................................18

Introduction.....................................................................................................................................18

Definition of pathways according to the CBD..................................................................................18

Definition of pathways in the IPPC framework................................................................................19

Definition of PRA and pathway PRA in the IPPC framework............................................................19

Types of pathway risk analysis in the IPPC framework....................................................................20

Control points in P-PRA...................................................................................................................21

Organism-based pathway risk analysis............................................................................................21

Commodity-based pathway risk analysis.........................................................................................22

Pathway(s) assessment and analysis...............................................................................................22

Pathway model(s)............................................................................................................................23

Assessing and prioritising pathways: the Euphresco project report................................................24

OIE Experiences/practices beyond IAS................................................................................................26

Pathogens in aquaculture................................................................................................................27

Closing remarks...................................................................................................................................28

References...........................................................................................................................................28

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IntroductionCurrent invasive alien species (IAS) policies are focussing on priority species, however priority pathways also need to be addressed. To identify priority pathways, these need to be analysed and their risks assessed.

This note summarises existing literature and experiences on assessing pathway risks and prioritising pathways, including experiences/practices beyond IAS (e.g. IPPC, OIE).

Sources include articles and reviews in technical and scientific journals, internet searches, online databases, grey literature and relevant books as well as personal communications with scientists, stakeholders, conservation practitioners and governmental bodies. A full bibliographic list detailing the literature and sources considered is included.

In particular, the description of the methodologies adopted in the selection of works reported in this note is excerpted from the relevant papers and technical reports, which the reader is invited to access directly for any additional information and/or clarifications.

Note: it was not possible to make a comprehensive analysis of the studies and procedures in place at the OIE in order to analyse, assess the risks and prioritise those pathways of introduction and spread of pathogens and diseases. This was due to the animal health experts contacted not being able to provide clarifications or inputs because of lack of time and resources. In addition, there is a risk of misunderstanding and confusion in relation to pathway analyses carried out in fields other than biological invasions due to (subtle) differences in the applied concepts and terminology. For this reason, only a generic description is provided.

The pathway analysis, as defined by Nobanis (2015), is a study that identifies which human activities have caused the introduction of alien species already present in the participating countries and territories. It also examines the taxonomy, invasiveness and origin of the introduced species, along with the changes of the introductions over time.

As a remark, a first comprehensive note on “Prioritising Pathways of Introduction and Pathway Action Plans” was prepared in January 2018 by a Working Group on Invasive Alien Species (WGIAS) established within the European Commission (WGIAS 2018). The document presents a voluntary guidance to aid in carrying out a pathway analysis and identifying pathways where priority action is needed. The WGIAS’s note also provides methods for classifying and prioritising pathways of introduction and spread of invasive alien species. It is a very comprehensive document, and therefore the present technical note includes parts of it, which are excerpted and further elaborated.

The same applies to the position paper on “Progress toward pathways prioritization in compliance to Aichi Target 9” prepared by the Invasive Species Specialist Group of the International Union for Conservation of Nature (ISSG-IUCN) and circulated for information by the Subsidiary Body on Scientific, Technical and Technological Advice (SBSTTA) at its 20th meeting (Scalera et al. 2016). An important document is also the “Guidance for governments concerning invasive alien species pathways action plans” presented at the 36th meeting of the Standing Committee to the Bern Convention held in Strasbourg, on 15-18 November 2016 (Scalera and Genovesi 2016).

The documents mentioned above provide a comprehensive review of the state of the art in relation to the methodologies adopted to analyse and prioritise pathways, as well as key challenges and

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possible solutions. Most elements are still currently valid and some are reported in this note. However, for a full appreciation of the issue, it is recommended to refer to the original documents.

As pointed out by WGIAS (2018) “At present, the most useful method is probably a combination of the methods for determining impact of IAS and quantification of pathways (volume of IAS, frequency of introductions, characteristics of the receiving environment, etc.) developed in cooperation with the CBD and described by Essl et al. (2015) and Blackburn et al. (2014)”. WGIAS (2018) also stressed that “If data is not available to carry out a pathway analysis using the method described above by Blackburn et al. (2014), an alternative could be a method that considers the frequency of IAS using a pathway, weighed together with the actual and potential impacts of the IAS using the pathway, similar to the approach of Madsen et al. (2014) and Nobanis (2015)”.

Main elements to consider in pathway analysis and prioritisation Presented in this section is a compilation of key elements to consider for the analysis and the prioritisation of pathways excerpted from the document prepared by WGIAS (2018), considered useful as a basis for the material reported in the following sections.

A more general approach to prioritising pathways is referring to the volume of IAS that enter the EU through a particular pathway or the impacts of the species. The volume of species (which includes the number of individuals transported through that pathway and the number of introduction events) is a coarse measure of the propagule pressure that the pathway presents. The propagule pressure is the number of individuals introduced in a single introduction event (propagule size) and the frequency of introduction events (propagule number) of an alien species entering an environment, which gives an indication of the potential risks posed by introducing species that may establish and become invasive through a pathway. Variables needed to quantify the propagule pressure (see also Hulme 2009, for additional details) include:

what species at the point of export could be transported through goods or other manner of transport and become invasive in the receiving country;

the frequency that this mode of transfer could occur; the survivorship and population growth of the alien species in transport; climate matching in the receiving environment to determine the probability of the species

establishing; the effectiveness of management measures to deter introduction; and the possibilities that the species will spread from the initial point of entry.

Unfortunately, information on the volume of IAS carried by a particular pathway is only available for a very limited number of pathways. The volume of IAS that a particular pathway carries can be estimated by considering transport routes, import statistics for various commodities that are associated with alien species (for example, as a contaminant of a commodity) or areas planted with an associated species (Essl 2015).

The most common method for prioritising pathways of introduction of IAS has been to analyze the number of alien species or IAS that have been introduced through different pathways (CBD 2014, page 7-9), also referred to as ‘frequently used pathways of introduction’. The output of this analysis will be a list of pathways and the number of introduced species via the different pathways. An advantage of using the method of frequently used pathways is that the data is generally available to produce this information. This method also gives an approximation of the propagule pressure that identified pathways may have.

Difficulties in using this method include:

the magnitude of impact of an IAS introduced through a particular pathway is not considered,

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many alien species may be introduced, but only a fraction establish and become invasive, there is often a lack of knowledge and uncertainties about the pathway of introduction of a

species (Essl et al. 2015), there may be multiple pathways of introduction for a species, and the importance and relevance of pathways may change with time.

Potential impacts of the species should also be considered. Individual pathways may allow for a large volume of movement or a large number of species to enter the given area, but an understanding of the impact those species are having, or may have in the future, is essential to prioritise pathways with the greatest negative impact. The output of this analysis is to define the invasiveness of a species and/or taxonomic group of species in relation to the pathway of entry. Priority pathways can then be highlighted based on the invasiveness of species entering through them.

Information on the impacts of IAS is perhaps easier to assess than the volume, but requires knowledge of what species enter through the different pathways, as well as how the pathway functions.

The CBD recommends that prioritisation of pathways should go beyond identification of the most frequent pathways of introduction to also include feasibility of management, conservation benefits and the likelihood of management success for a given level of investment (cost-effectiveness) and social preference (CBD 2014b, Dawson et al. 2015, Scalera 2015).

Economic costs of the management could also be weighed into the prioritisation process.

A method of prioritising conservation benefits and technical feasibility of management measures has been used for prioritising islands for IAS eradication measures (Dawson et al. 2015), but could also be used for prioritising pathways of introduction. The advantage of this method is that conservation values of biological diversity and related ecosystem services would be the central focus in the prioritisation. Dawson et al. (2015) assigned potential conservation benefits to islands using an index based on the value of all potential conservation values for each native species that would benefit from the eradication of invasive vertebrates. The potential conservation value included scores taking into account the threat status (according to the IUCN Red List) and irreplaceability of native species, severity of impact, and possibility for reintroduction of extirpated native species. The feasibility score was assigned from criteria including the size and geographic features of the island, which may complicate eradication, human population size on the island, and expert opinion on possibilities of success using the eradication measures recommended by eradication experts. Economic costs were not weighed into the prioritisation, but a measure of cost-effectiveness could be included. Some development of this method will be necessary before using it in prioritising pathways of introduction, but it is clearly a potentially useful approach.

In conclusion, the WGIAS (2018) formulated the following recommendations for prioritisation of pathways:

1. Methods for prioritising pathways are being rapidly developed. At present, the most useful method is probably a combination of the methods for determining impact of IAS and quantification of pathways (volume of IAS, frequency of introductions, characteristics of the receiving environment, etc.) developed in cooperation with the CBD and described by Essl et al. (2015) and Blackburn et al. (2014). These methods ensure a standardization of the prioritisation results that can be compared with other countries and regions. Unfortunately, this method requires a large amount of data that are presently not available for the majority of pathways.

2. Using simpler methods and proxy information for missing data is perhaps the reality in prioritising most pathways. Recommended methods are those that consider the frequency of IAS using a pathway weighed together with the actual and potential impacts of the IAS

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using the pathway, similar to the approach of Madsen et al. (2014) and Nobanis (2015). Including conservation values for managing the pathways and feasibility of management would add a greater value to the prioritisation results, but this approach requires further testing.

3. It is important to consider both the volume of the alien species transported through a pathway, which includes the number of individuals transported through that pathway and the number of introduction events, as well as the actual impacts of the species. Potential impacts of the species should also be considered.

4. Ecosystem services are not considered in any of the described prioritisation methods. Methods should be further developed to include the value of ecosystem services and impact of IAS on them when prioritising pathways of introduction.

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Main works supporting the development of methodologies for pathway analysis and prioritisationMcGeoch et al. (2016) define prioritization of pathways as the process of ranking species, pathways or sites for the purposes of determining their relative environmental (and sometimes also socio-economic) impacts and deciding on the relative priority of actions that effectively and efficiently prevent or mitigate the impact of biological invasions. McGeoch et al. (2016) also stress that the process of prioritization in biological invasion happens for two distinct purposes and encompasses risk assessment (RA), although both purposes can be addressed simultaneously. Existing prioritization schemes vary widely in the relative emphasis given to one or both of these purposes. Prioritization is often based on the results of a risk assessment, which may be formal or informal, qualitative, semi-quantitative or quantitative, and is sometimes formally incorporated as the desired end point of a risk assessment process (Leung et al. 2012). For unintentional introductions, species based prioritization is not always feasible because which species will arrive is difficult to predict, and the biology and life history of the species that do arrive are sometimes poorly known (Leung et al. 2014). The focus on species must therefore be balanced with a focus on pathways of introduction and spread, with the purpose of preventing the propagules that they carry from arriving and spreading (Hulme 2009). Prioritization of pathways uses information on the full suite of vectors and routes by which alien propagules are introduced, and the propagule loads of such pathways (Carlton and Ruiz 2005, Hulme et al. 2008, Essl et al. 2015). There are two ways in which a particular pathway may be prioritized:

(1) according to the number of different invasive species that are introduced and spread by the pathway, and

(2) based on the severity of the impact caused by the invasive species introduced and spread by the pathway (Essl et al. 2015).

The latter would use species risk assessment information to determine which pathways are associated with species with the greatest magnitude of impact.

The following table provides information needed by countries for prioritizing pathways, according to McGeoch et al. (2016). (For details and references please see relevant paper):

Data collation and scoping Surrogates, in the absence of data or incomplete data for the country

Examples of question-based criteria for prioritization

List the full range of pathways for introduction of alien species relevant to the country, both potential and realized

Introduction deliberate or accidental?

Frequency, number, and identity of alien propagules entering, transported, or spread via each pathway (e.g., based on interception records

Climatically matched sources of potential origin linked to country via one or more pathways.

Volumes or frequency of goods, products, or people moved via pathways

Pathways known to be important in other countries or globally

Expert judgment

How relevant and important (based on degree of activity) to the country are the following pathways?

- Release (e.g., biological control)

- Escape (e.g., via horticulture)

- Transport (contaminant) (e.g., with timber trade)

- Transport (stowaway) (e.g., ballast water)

- Corridors (e.g., rivers)

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As summarised by the CBD (2014a), regarding the analysis on the routes and means of arrival into a new biogeographic region and targeted site, key steps in a pathway prioritization should include the following:

Identify casual chains between a putative pathway and levels of invasion in the region of interest;

Assess the diversity, abundance and survivorship of invasive alien species along the pathway;

Describe how the pathway risk is changing both spatially (in terms of suitability of different regions), taxonomically and temporally (rate and magnitude of potential introductions);

Distinguish between pathways where introduction may cause high impacts from those where impacts will be minor;

Present means to assess and implement means to mitigate the problems posed by the pathway; and

Identify new and emerging pathways.

Unfortunately, the data and information required to carry out a pathway analysis as described by the CBD (2014a) are rarely available, as pointed out by WGIAS (2018), according to which those carrying out analyses of pathways will need to use a pragmatic approach and use available information and proxies, while clearly indicating uncertainties (CBD 2016).

Essl et al. (2015) have designed a standardised, hierarchical categorization of pathways and associated measure of size or severity of risk associated with each pathway category, for all taxa and pathways. The same authors also described some variables that need to be considered in the analysis of pathways for policy and management purposes.

As summarised by Scalera et al. (2016) the potential to conduct sound analysis using pathway data in major databases (Katsanevakis & Roy 2015) is limited by the disparate terminology to describe the same pathway, and in most cases also by differences in the scope and intention of these databases, i.e. temporal and spatial scale, taxonomic groups, and environments (Essl et al. 2015). Saul et al. (2017) investigated the implications of such differences for the prevention of introductions and for prioritization of pathways in management and surveillance, by collating pathway information from two of the main global datasets: GISD (updated version http://www.iucngisd.org/gisd/) and DAISIE (http://www.europe-aliens.org). Apparently, the available pathway databases may have limited value in combatting biological invasions given the high uncertainty with which species are often assigned to a pathway, and the retrospective approach in assignments, which may be invalid where the importance of different pathways shifts over time (Hulme 2015). Another constraint on the potential for sound assessments of pathway risks (e.g. to predict relevant trends) is the complexity of the network which may characterize the target pathway. In general, the key information needed for the analysis is rarely available for more than a few specific pathways and for a very limited number of species. Such variables are also difficult to measure given their very dynamic nature. Thus, the assessment of pathway risks needs to rely rather on proxies for propagule pressure (Essl et al. 2015). The importance of pathways over space and time may vary because of complex interactions between the environment and socio-economic factors, e.g. depending on the functional traits of the introduced species, trade routes, and other factors, which might have major implications in terms of management and effective prevention of future invasions (Essl et al. 2015, Hulme 2015, Saul et al. 2017). Assigning the entry or spread of alien species to specific pathways may be subject to various levels of uncertainty and, while in some cases there is excellent evidence supporting the global significance of some pathways, for some areas/pathways there are important gaps e.g. the only available information may be based on expert opinion rather than on evidence (McGeoch et al. 2016), and data might need to be extrapolated from regions where comprehensive documentation is available, to areas where the documentation is not as clear. Otherwise, in some

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cases, the exact pathway responsible for a particular introduction may be simply unknown (Essl et al. 2015).

Overall, although evidence-based input is highly desirable, prioritization is possible in cases where data are scarce: even without baseline data, the combined use of expert opinion and evidence from elsewhere can help prioritization activities, according to McGeoch et al. (2016).

In fact, McGeoch et al. (2016) suggest considering the opportunity to make integrated prioritization more explicit, i.e. quantitative integration of priorities across multiple species, pathways, and sites. This could be achieved by identifying combinations of factors that jointly warrant priority attention, regardless of how the component factors have been classified. In particular, this would allow to address questions that have been little addressed to date. For example: which pathways are associated with the introduction of multiple highest-priority species at sensitive sites, or which sites (or categories of sites) are most susceptible to invasion by those same species?

Leung et al. (2012) provide some clarifications in relation to the transport and introduction component of the invasion process, by critically discussing the contribution of variables such as propagule pressure, which may vary according to the vector and pathway characteristics, destination environment, species traits, vulnerability of the site to colonisation, etc. The authors note that the subcomponents associated with propagule pressure will often not be measurable directly, and surrogate measures using accessible data may be needed. For instance, volume of trade and human population size may be relevant correlates of vector traffic and characteristics of source populations and extent of spread in source areas may correlate with uptake. However, in situations where actual numbers of individuals introduced or release events are known, Leung et al. (2012) suggest that there is no need to estimate transport, given that a direct measure of propagule pressure is already available.

For example, in a study on patterns of transport and introduction of exotic amphibians in Australia García-Díaz & Cassey (2014) expected unintentional transport of amphibians to be strongly influenced by the mobility of people, goods and services within and to Australia. For this reason, for their pathway analysis, they took into account data on the average value of imports, the annual average number of seats per airplane and the annual average number of airplanes flying to Australia.

Also the Guidelines for Conducting Pathway Assessment (Orr and Fisher 2009) provide an outline of the flow of a pathway analysis, dividing the process into initiation, risk assessment, and risk management (where the need for a risk assessment starts either with the request for opening a new pathway that might harbour aquatic invasive organisms, or the identification of an existing pathway that may be of significant risk). According to Orr and Fisher (2009), all pathways showing a potential for non-indigenous organism introduction should receive some degree of risk evaluation. Those pathways that show a high potential for introducing non-indigenous organisms should trigger an in-depth risk assessment. Specific information needed about the pathway will vary with the “type” of pathway (e.g., ballast water, aquaculture, aquarium trade, fish stocking). The following generalized list of information has been useful in other non-indigenous species? risk assessments:

1) Determine exact origin(s) of organisms associated with the pathway.2) Determine the numbers of organisms traveling within the pathway.3) Determine intended use, or disposition, of pathway.4) Determine mechanism and history of pathway.5) Review history of past experiences and previous risk assessments (including foreign

countries) on pathway or related pathways.6) Review past and present mitigating actions related to the pathway.

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There are also other key issues to consider, as highlighted by WGIAS (2018), such as: Including conservation values of managing the pathways and feasibility of management

would add a greater value to the prioritisation results, but this approach requires further testing;

Methods should be further developed to include the value of ecosystem services and impact of IAS when prioritising pathways of introduction.

It is worth pointing out that the management feasibility component is particularly relevant for the prioritisation exercise, because assessing if target pathways can be effectively managed to minimize the introduction of IAS is key, given the limited resources and time usually available (WGIAS 2018).

Examples of analyses made at the European levelA recent work on IAS pathway analysis at the European level was carried out by Pergl et al. (2017). The authors addressed the knowledge gap between impact and introduction pathways by relating, for the first time, the pathways of introduction of alien species spanning a range of taxonomic groups (plants, mammals, freshwater fish, and terrestrial invertebrates) in Europe to their ecological impacts. The aims of this study were:

(i) to explore whether species with known ecological impacts differed in their pathway associations from those species for which no impact had been reported;

(ii) to identify for particular alien taxonomic groups which pathways posed the greatest threat;

(iii) to explore whether species transported by multiple pathways were associated with a higher probability of impact.

More generally, the study presents a first attempt to identify the most relevant pathways of introduction of IAS with impact. The study highlights that the proportions of alien species with negative ecological impacts are taxon-specific, a finding that should be reflected in legislation and pathway management. However, in many cases at the present level of understanding, the best predictor of the relevance of an introduction pathway is the total number of species that are associated with it. Furthermore, the study showed that its results are highly dependent on the availability of data, and that it is necessary to better reflect the scales of impacts ranging from minimal to massive to improve understanding and management of IAS. For most taxa it was not possible to detect major differences in the way in which IAS arrive. Therefore, the authors suggest that, until robust and comprehensive information on impact is available, we should not focus on subtle differences between the pathways of arrival for different taxonomic groups, but instead consider the most common pathways for all taxa and pathways that are most easily managed. Thus, pathways that deliver many species should become a management priority.

Examples of recent analyses made in Europe at the country/region levelIn Europe, studies on pathway analysis and prioritisation for invasive alien species are publicly available only for a few countries/regions, i.e. Nordic countries (Nobanis 2015), Denmark (Madsen et al. 2014), Ireland and Northern Ireland (Kelly et al. 2013). However, other studies are being finalised in view of the deadline of 1 June 2019 for reporting to the Commission on the implementation of Regulation (EU) No 1143/2014. A concise summary of the approach characterising the three studies mentioned is presented below.

Nobanis (2015) analysed IAS pathways at a regional level (three regions: a Nordic region consisting of Denmark, Finland, Norway, Sweden and Svalbard; a Baltic continental region consisting of Estonia, Latvia and Lithuania; and a region consisting of the islands in the North Atlantic Ocean represented by Iceland and the Faroe Islands). In this study, the NOBANIS database has provided the basis for the pathway analysis, and each country updated their national data with information available using

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relevant literature and articles, and by consulting national experts. Besides the identification of the human activities known to have caused the introduction of IAS occurring in the target region, the taxonomy, impacts and origin of the introduced species, along with the changes in patterns of introductions over time, were also investigated. In particular, the prioritization method used in this study considered as a key parameter the number of “door knocker” species (species not yet recorded, but suspected to be at high risk of arrival) identified by the ad hoc horizon scanning exercise, and the pathways associated to those species.

As summarized by WGIAS (2018), the factors considered to rank pathways in the Nobanis study were: number of alien species that use a pathway, percentage of the alien species using a pathway that are invasive, and the number of IAS identified in the horizon scanning as being ‘high risk’ and ‘medium risk’, as well as ‘potentially invasive’. A complication in the analysis was that pathways of introduction for a great number of IAS are still unknown and many species have multiple pathways of introduction. More in detail, the pathway analysis contains the following subanalyses:

Pathways of introduced species. Invasiveness of introduced species. Taxonomic groups of introduced species. Temporal development of pathways. Species origin and the pathway of introduction.

In the process of prioritising pathways of concern, Nobanis (2015) looked at the results from the pathway analysis. In particular, the prioritisation was done based on:

Number of introduced invasive species by the pathway. Number of introductions through the pathway.

Subsequently, other parameters from the pathway analysis (and the horizon scanning, which was part of the study) were taken into account to make adjustments to the prioritisation of the pathways:

Percentage of invasive introductions = (invasive introductions by that pathway/all introductions by that pathway) x 100).

Number of high risk (A) door knocker species that is assigned to the pathway. Number of medium risk (B) door knocker species that is assigned to the pathway. Number of potentially invasive introductions. Temporal development of pathways.

Madsen et al. (2014) analysed the IAS pathways for Denmark. In this case, pathways of introduction were identified on the basis of the categories defined in the NOBANIS database from which most data were retrieved, e.g. taking into account the pathways of introduction, the mode of entry, and the type of introduction for each species. In particular, the following analyses were made:

Analysis of the identified Pathways of Introduction, Mode of Entry and vectors (performed for each species group);

Identification of the most common pathways, modes and vectors (performed for each species group);

Analysis of Pathways of Introduction (performed across all species groups).

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Additionally, the impact of each species was analysed on the basis of the Harmonia+ guidelines. In particular, as summarized by WGIAS (2018), Madsen et al. (2014) examined the degree of invasiveness for a selection of IAS relevant to Denmark, using the Harmonia index (Branquart 2007) and considering: dispersal potential, colonization of high conservation value habitats, adverse impacts on native species and alteration of ecosystem functions. Economic impacts and human health impacts were also considered. Each of the species analysed were then placed into categories of species with high scores or greatest impact (Harmonia index score 14-18), medium impact (11-13), and lesser impact (6-10). The pathways of introduction were then prioritised by considering the percentage of the species examined in the study that use a pathway, and then being weighed by their environmental impact score. The study confirmed the generalized lack of knowledge on pathways of introduction for many species.

Kelly et al. (2013) made a preliminary pathway analysis in Ireland and Northern Ireland. The analysis of IAS pathways focuses on the number of species per pathway. The results presented in the study relate only to the species overall risk rating, as defined by the scoring system, and their association with pathways. The analysis of habitats, pathways, date of introduction and other factors will be the subject of an additional report prepared by the National Biodiversity Data Centre and ISI (Invasive Species Ireland).

Other studies are being undertaken by EU Member States in view of the deadline of 1 June 2019 for reporting to the Commission on the implementation of Regulation (EU) No 1143/2014. However, they are not yet available. For example, some studies were made in Cyprus, but are not yet publicly available (Bakaloudis and Tsipripidis 2017). The pathway analysis was done for the first batch of 37 IAS of Union concern and then for the second batch of 12 IAS. The first analysis was much more elaborate and detailed. In particular, all the information from the Cypriot state agencies, as well as data from global databases (e.g. GISD, NOBANIS, EPPO, CABI, NNSS GB, DAISIE, etc.), were used in the study of the 37 IAS regarding: pathways of introduction, mode of entry, import mechanism, mechanism of introduction, and type of import introduction. An evaluation was also carried out for the 37 IAS based on the Harmonia+ and the EICAT systems. The study also included a statistical analysis on the values obtained for the different categories of pathways (because the distribution was not normal, a cut-off at the 25th and 75th percentiles was used to identify low, medium and high priority pathways).

Also, building on the results of Kelly et al. (2013), another methodology is being developed for Ireland to illicit pathway priorities based on the list of 49 species of European concern, although data are not yet available (C. O'Flynn, pers. comm. 2019). Similarly, studies on the issue are also being prepared in other countries, although the methodology is still being fine-tuned, e.g. in Italy (L. Carnevali, pers. comm. 2019) and Slovenia (M. de Groot, pers. comm. 2019). As pointed out by WGIAS (2018), using simplified approaches, such as those used by Madsen et al. (2014) and Nobanis (2015), will probably be necessary in the first round of pathway analyses. Member States and other relevant organisations should actively work to improve knowledge on impacts and pathways of IAS, and repeat pathway analyses as more information becomes available.

Pathway analyses of alien species in freshwater environmentsPanov et al. (2009) developed a conceptual model of risk assessment of IAS introductions via European inland waterways. Because of the high degree of scientific uncertainty when dealing with such a global and complex ecological issue as large-scale intercontinental and intracontinental introductions of non-native species, a qualitative model was selected for risk analysis of alien species introductions via European inland waterways. It includes seven main components:

1. Identification of main invasion gateways, routes, and corridors in Europe;

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2. Selection of ecosystems as assessment and management units (assessment units) within invasions corridors/invasion network;

3. Identification and analysis of pathways of alien species introductions within the ecosystem-‘‘driving forces’’ according to the driving forces–pressures–state–impact-response (DPSIR) framework;

4. Assessment of inoculation rates (propagule pressure) within the ecosystem-DPSIR ‘‘pressures’’;

5. Assessment of biological contamination of the ecosystem-DPSIR ‘‘state’’;6. Assessment of invasiveness of alien species, established in the ecosystem (biological

pollution risk)-DPSIR ‘‘impacts’’;7. Development of an online Risk Assessment Toolkit with early warning service for reporting

of environmental indicators and recommendations for risk management to stakeholders-DPSIR ‘‘responses’’.

Pathways involved in the introductions of IAS can be considered as ‘Driving forces’ according DPSIR framework. “Driving forces” are changes in the social, economic and institutional systems which are triggering, directly or indirectly, the creation of invasion corridors resulting in the introduction of IAS (Maxim et al. 2007). Principal pathways and the dispersal vectors of invading aquatic species in Europe have been identified (Minchin et al. 2007), as have qualitative descriptors of principal human activities involved in non-native species dispersal (see Panov et al. 2009, for details). For the purpose of the qualitative risk assessment of IAS introductions via inland waterways, all of these principal human activities were considered as potential pathways for any selected ecosystem (as an assessment unit). Pathways are defined according to three classifications.

1. A pathway with low certainty of the existence of a specific pathway for a specific assessment unit can be defined as a ‘‘low-risk pathway.’’

2. A pathway with a high level of certainty of its existence in the assessment unit (as defined by the descriptors for the operating pathway in Panov et al. 2009) but with no evidence of the introduction of alien species into the assessment unit by this pathway during the observation period, can be defined as a ‘‘high-risk pathway.’’

3. Where the operating pathway can be defined as responsible for an introduction of a specific alien species into an assessment unit during the past 10 yr (even if only 1 record of alien species within this period can be accounted for with some level of certainty to the specific pathway), it can be defined as an ‘‘extreme-risk pathway.’’

The 2nd stage of pathway analysis includes the estimation of potential species-specific pathways for alien aquatic species introduced into European inland, transitional, and coastal waters via inland waterways that can be further used for estimation of species invasiveness (see discussion in Panov et al. 2009, for details).

Also Nunes et al. (2015) made an analysis of the main pathways and gateways of introductions of freshwater alien species in Europe, which included an assessment of the spatial and temporal patterns and trends of biological invasions in freshwater ecosystems in Europe, in relation to different pathways. The study built on the inventory of freshwater alien species present in Europe archived by the European Alien Species Information Network (EASIN) and the classification of pathways suggested by Hulme et al. (2008). The study was the first European-wide assessment of both the major pathways and gateways of first introductions for freshwater alien species in Europe. In particular, the number of initial introductions of freshwater alien species in Europe, as well as temporal trends of these invasions, in relation to different pathways of initial introduction, was

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assessed. The main gateways (i.e. recipient countries) of species introductions in Europe, and associated pathways per country, were also analysed. Finally, the number of introductions for each of the most common introduced freshwater taxa, considering the different status of alien species (established, cryptogenic and questionable) and different pathways of introduction, was investigated. It also considered patterns for species partly native to Europe and on so-called ‘high-impact’ introduced species (see Nunes et al. 2015 for details).

Tricarico (2012) made a review on pathways and drivers of use regarding non-native freshwater fish introductions in the Mediterranean region. For this purpose, key datasets, peer-reviewed literature and technical reports were consulted to extract information on the non-native species introductions in the inland waters of the Mediterranean area. For each species, the following categories of information were collated: native range, date of introduction in each country, current distribution in the Mediterranean region, mode(s) of arrival in each country (i.e. accidental or intentional introduction), pathway(s) and driver(s) of use associated with the introduction, and current status (i.e. established/not established).

Pathway analyses of alien species in marine environmentsKatsanevakis et al. (2013) made an assessment of pathways of introduction of marine alien species in European seas. Based on their reported year of introduction, trends in the numbers of introduced species per pathway/vector were assessed on a decadal basis and invasion patterns were described for each pathway. The classification of pathways of introduction was based on the frameworks proposed by Hulme et al. (2008) and Molnar et al. (2008). An inventory of marine alien species in Europe (in the broad sense, i.e. including all EU and non-EU countries mentioned in http://europa.eu/about-eu/countries/) was created by critically evaluating related information in European, regional, and national online information systems on alien species in Europe (this inventory is part of the European Alien Species Information System (EASIN; Katsanevakis et al., 2012)).

The link between species and pathways was based on scientific literature, i.e. on published justification by experts of why a species is believed to be introduced via a specific pathway. In cases of uncertainty or diverging opinions among experts, literature was critically evaluated to reach a decision. In some cases, the pathway was defined by expert judgment as the best plausible alternative. A modification of the approach proposed by Minchin (2007) was applied, according to which for each species one of the following uncertainty categories on the pathway(s) of introduction is relevant:

(1) There is direct evidence of a pathway/vector: The species was clearly associated to a specific pathway/vector at the time of introduction to a particular locality. This is the case e.g. in all intentional introductions (i.e. aquaculture/commodity) and in many cases of Lessepsian immigrants (when there was direct evidence of a gradual expansion along the Suez Canal and then in the localities around the exit of the Canal in the Mediterranean).

(2) A most likely pathway/vector can be inferred: The species appears for the first time in a locality where a single pathway/vector(s) is known to operate and there is no other rational explanation for its presence except by this pathway/vector(s). This applies to many species introduced by shipping or aquarium trade or as aquaculture contaminants. In some cases, a specific vector could not be inferred, e.g. some species probably introduced by shipping could not be further linked to ballasts or hull fouling and were classified as ‘shipping/unknown’. In many cases inference is based on known examples of introductions elsewhere for the same or similar species, the biology and ecology of the species, the habitats and locales it occupies in both the

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native and introduced range, and its pattern of dispersal (if known), e.g. for a fouling species frequently recorded in/near ports, shipping has been assumed to be the most probable vector.

(3) One or more possible pathways/vectors can be inferred: The species cannot be convincingly ascribed to a single pathway/vector. Inference is based on the activities in the locality where the species was found and may include evidence on similarly behaving species reported elsewhere.

(4) Unknown: Where there is doubt in relation to any specific pathway explaining an arrival.

The authors pointed out that the date of the introduction of a species into a new locality is important for the study of the patterns and processes of invasion, but that it is difficult to ascertain for unintentional or undocumented intentional introductions.

Similarly, Zenetos et al. (2012) made a study on pathways in the Mediterranean Sea. In particular, trends in pathways of introduction in the Mediterranean, represented by the number of new alien species per decade and per pathway of first introduction, were analysed . The focus was on the pathways of the first introduction in the Mediterranean since 1950 and have not considered pathways of subsequent transfers to other areas. The link between species and pathways was based on scientific literature, i.e. on published justification by experts. In cases of uncertainty or diverging opinions among experts, literature was critically evaluated by the authors to reach a decision. In some cases, the pathway was defined by expert judgment as the best plausible alternative. A modification of the approach proposed by Minchin (2007) was applied, according to which, for each species, one of the following is true:1) There is direct information of a pathway (uncertainty category 1). The species was clearly

associated to a specific vector(s) of a pathway at the time of introduction to a particular locality.2) One most likely pathway can be inferred (uncertainty category 2). The species appeared for the

first time in a locality where a single pathway is known to operate.3) One or more possible pathways can be inferred (uncertainty category 3). The species cannot be

convincingly ascribed to a single pathway.4) Unknown: There is doubt in relation to any specific pathway explaining the arrival of the

species.

Zenetos et al. (2018) made also an analysis through an extensive literature survey of the primary pathways of introduction in Greek waters only. The following data were also provided for each introduced species listed:

- Updated nomenclature;- Date (year) of the first finding in Greece;- Alien, cryptogenic, or debatable status;- Population Status (= Establishment success) in Greece;- Most plausible pathway(s) of introduction in Greek waters, according to the CBD

classification (UNEP 2014).

The link between species and pathways was based on scientific literature, i.e. on published justification by experts of why a species is believed to be introduced via a specific pathway. More than one pathway/vector was assigned to a species when different introduction events by different pathways/vectors occurred within Greek Seas. A degree of certainty was assigned to each pathway according to Katsanevakis et al. (2013).

Other examples of pathway analyses Kraus (2007) conducted analyses to assess the pathways by which reptile and amphibian species were being transported and to determine how those pathways have varied (i.e. a risk assessment of

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pathways for taxa introduced accidentally). The study is based on a database of alien reptile and amphibian introductions worldwide built by the author. Data collected, when available, included the jurisdiction to which the species was introduced, date(s) of introduction, pathway(s) of introduction, minimum number of introductions involved, and whether the introduction led to a currently established population. Jurisdictions were typically countries but distinct island groups were tracked separately from the remainder of the country (e.g. Galapagos separate from Ecuador, Ryukyu and Ogasawara archipelagos separate from Japan) and species were tracked by state and province within the US and Canada. From these data, analyses were conducted to assess the pathways by which herp species were being transported and to determine how those pathways have varied. The same literature was reviewed to assess what ecological and economic impacts have been reported for alien herp introductions and what control measures have been attempted to date.

Pyšek et al. (2011) used the alien flora of the Czech Republic, Central Europe, for which comprehensive information exists on various aspects of invasions to explore:

(i) how many alien species were introduced by different pathways and whether the pattern of these introductions has changed over time;

(ii) whether species introduced by certain pathways are more likely to become invasive, more widespread or occupy a wider range of habitats, and

(iii) whether pathways can be related to species traits, i.e. are species with certain traits predisposed to introduction via a particular pathway more so than via other pathways?

Faulkner et al. (2016) assessed the South African introduction pathways in terms of the number of introductions, the invasion success of introduced taxa, how the pathways have changed over time, and how these factors vary for vertebrates, invertebrates and plants.

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Pest Risk Analysis and Pathway Risk Analysis in the IPPC context

Pest Risk Analysis and Pathway Risk Analysis are well defined procedures in the IPPC context and clearly used as a framework by a number of International Standards for Phytosanitary Measures (ISPMs). Most Regional Plant Protection Organisations (RPPOs) and National Plant Protection Organisations (NPPOs) have adapted these basic IPPC standards in carrying out their PRAs and Pathway RAs. There is of course both a dichotomy and an overlapping area within the PRA process of whether phytosanitary threats (or invasive alien species) should be addressed by putting an emphasis on the organisms or on the pathways on which they are carried and spread. The existing base techniques can be supported and improved using specific software, adequate expert elicitation techniques, additional model and experimental tools including dedicated infrastructures and sentinel gardens.

IntroductionPathway (pest) risk analysis can be defined as an expert-based standard procedure that involves identifying a set of relevant or potentially relevant pathways, assessing the risks 1 associated with each pathway, and evaluating the ease with which each pathway might be managed. With respect to a specific set of (invasive) alien species and pathways, the outcome of the technique is a smaller set of high-risk pathways that account for a large proportion of invasive species introduction and spread, and for which effective management programs may be put in place to avoid or reduce substantial negative impacts on protected assets and ecosystem services. Although many different types of software and tools can support the analysis, the procedure is so far mostly expert-based.

Pathway (pest) risk analysis may be used for a variety of purposes; for example, to identify potential pathways for the introduction and spread of pests (or alien species), to assess the likelihood and consequences of the introduction or spread of pests along a pathway, to compare and rank multiple pests and pathways according to their level of risk, and to identify risk management options and evaluate their efficacy (NAPPO 2012).

Definition of pathways according to the CBD A standardized pathway terminology and classification was first proposed by Hulme et al. (2008). Lately, a unified system to categorise introduction pathways of invasive alien species was proposed in the document of the Convention on Biological Diversity (CBD) on “Pathways of introduction of invasive species, their prioritization and management” (UNEP 2014)2. The CBD pathways categorization distinguishes intentional and/or unintentional introductions, and the introduction mechanism as either the importation of a commodity, arrival via a transport vector, the establishment of an anthropogenic dispersal corridor, or the natural spread from a region where the species is itself alien. These mechanisms are divided into six main categories: Release; Escape; Transport-contaminants; Transport-stowaway; Corridors; and Unaided. These six categories include a number of sub-categories3.

1 For a general definition of risk, CFR Stefan Schneiderbauer & Daniele Ehrlich (2004) Risk, hazard and people’s vulnerability to natural hazards – EU JRC Ispra, IT. EUR 21410 EN.

A review of definitions, concepts and data

2 https://www.cbd.int/doc/meetings/sbstta/sbstta-18/official/sbstta-18-09-add1-en.pdf

3 CFR UCN. 2017. Guidance for interpretation of CBD categories on introduction pathways. Technical note prepared by IUCN for the European Commission.

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Definition of pathways in the IPPC frameworkThe ISPM 5 (International Standards for Phytosanitary Measures) - Glossary of Phytosanitary Terms (International Plant Protection Convention 2007-2018)4 defines a pathway as “any means that allows the entry or spread of a pest [FAO, 1990; revised FAO, 1995]”. Please note that “Entry” is therein defined as the “movement of a pest into an area where it is not yet present, or present but not widely distributed and being officially controlled [FAO, 1995]”. Additional information is provided in the revised version of the ISPM no. 5 (2018), where “Unintentional introduction” is explained in IPPC context as the “entry of a non-indigenous species with a traded consignment, which it infests or contaminates, or by some other human agency including pathways such as passengers’ baggage, vehicles, artificial waterways”.

Definition of PRA and pathway PRA in the IPPC frameworkPest Risk Analysis (PRA) is a standard structured procedure to evaluate the risks from pests (including invasive alien species) and to suggest mitigation measures to manage any identified threats. Most countries use the IPPC generic guidelines, summarised through two main International Standards for Phytosanitary Measures (ISPMs), i.e.: (1) ISPM 2 – Framework for pest risk analysis (International Plant Protection Convention, 2007, 2016); and (2) ISPM 11 – Pest risk analysis for quarantine pests including analysis of environmental risks and living modified organisms (International Plant Protection Convention, 2004, 2017). However, additional ISPM standards have to be considered when performing a PRA, such as ISPM 5 - Glossary of phytosanitary terms (International Plant Protection Convention, 2018). Concerning this latter document, it is noteworthy that a new appendix was adopted by the Fourth Session of the Commission on Phytosanitary Measures in March–April 2009. Although this appendix is for reference purposes only and is not a prescriptive part of the standard, it provides relationships between the terminology of the Convention on Biological Diversity on invasive alien species and the Glossary of phytosanitary terms.

Most Regional Plant Protection Organisations (RPPOs) and National Plant Protection Organisations (NPPOs) have adapted these basic IPPC standards in carrying out their PRAs (Evans, 2010). In Europe, the European & Mediterranean Plant Protection Organisation (EPPO) and the European NPPOs tend to use a common template for PRA that has been modified regularly in recent years (EPPO, 2012). This includes the possibility to adapt the decision scheme aiming to evaluate whether to start or not the procedure, and the requirements of the Regulation (EU) no. 1143/2014 concerning the definition of “invasive alien species of Union concern” (Branquart et al. 2016). In addition, specific steps of the process are discussed and detailed in the scientific literature (e.g. Holt et al. 2014).

There is of course a dichotomy within the PRA process of whether phytosanitary threats should be addressed by emphasis on the organisms or on the pathways on which they are carried (Evans, 2010). Indeed, ISPM 2 and ISPM 11 specify that the Pathway Pest Risk Analysis (P-PRA) is initiated by concern about a pathway or pathways, rather than a species (FAO 2004-2017, FAO 2007-2016, Mumford & Leach 2009, Baker et al. 2009, Devorshak 2012). Therefore, in the IPPC context, pathway PRAs are used to describe and assess risks associated with the movement of commodities5 with such pathways as transport, people and living organisms that may result in the intentional or unintentional introduction of one or more pest organisms that threaten the health of plants in a defined pest risk assessment area. In the IPPC context, a pathway PRA leads to risk management that is specific to a particular pathway or several pathways and may address risks from several pests within the pathway(s).

Importantly, the North American Plant Protection Organization (NAPPO) developed science-based Regional Standards for Phytosanitary Measures which are intended to protect agricultural, forest and other plant resources against regulated plant pests, while facilitating trade. Among these

45 CFR ISPM 32 – Categorisation of Commodities According to their Pest Risk.

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standards, the NAPPO approved RSPM 31 "General Guidelines for Pathway Risk Analysis" states that pathway risk analysis, is a type of pest risk analysis (PRA), and is consistent with the obligations and rights of sovereign nations as described in the International Plant Protection Convention (1997), in particular at article 16. Also, the project PRATIQUE7 has provided new insights in the field of pathway PRA. PRATIQUE is an EC-funded 7th Framework research project designed to address the major challenges for pest risk analysis (PRA) in Europe. It has three principal objectives: (i) to assemble the datasets required to construct PRAs valid for the whole of the EU, (ii) to conduct multi-disciplinary research that enhances the techniques used in PRA and (iii) to provide a decision support scheme for PRA that is efficient and user-friendly. A specific Work package focusing on pathways was included (WP4. To refine methods for pathway analysis and systems approaches). The documents developed within the project are available here: https://secure.fera.defra.gov.uk/pratique/publications.cfm

Types of pathway risk analysis in the IPPC frameworkAccording to NAPPO (2012) the type of pathway risk analysis refers to whether the analysis considers one or multiple pests, and one or multiple pathways. Variation in these two factors results in four types of pathway risk analyses:

• Single pathway, single pest, (e.g., marble tile transporting a snail species);• Multiple pathways, single pest, (e.g., trade, tourism, and military equipment enabling the

movement of a pest between regions);• Single pathway, multiple pests, (e.g., commodity from one location with a number of associated

pests, plants for plantings from China to the EU);• Multiple pathways, multiple pests, (e.g., air and sea cargo from another country to the EU

carrying multiple pests; two country border analysis).

As stated in RSPM 31 (NAPPO 2012), at times, the difference between a pathway risk analysis and another type of pest risk analysis may not be obvious because they share somewhat similar objectives and methodologies. For example, single pathway - single pest analyses will sometimes resemble pest risk analyses, particularly when they include detailed consequences of introduction/spread. Also, single pathway - multiple pest analyses will sometimes resemble commodity-based pest risk analyses when the pathway is a commodity that is the pest host. In these cases, classification of the risk analysis as a pathway risk analysis or some other type of phytosanitary analysis is perhaps more of an academic exercise that has no bearing on the development or use of the analysis itself (NAPPO 2012). However, according to RSPM 31 "General Guidelines for Pathway Risk Analysis", a risk analysis can be considered a pathway risk analysis if the emphasis of the analysis is on the likelihood of introduction or spread.

The RSPM 31 (NAPPO 2012) describes the four stages in pathway risk analysis (initiation phase, pathway description, pathway risk assessment, pathway risk management). These stages are roughly analogous to the steps and stages of pest risk analysis described in ISPM 2 and ISPM 11 for PRA (initiation, pathway description, risk assessment, and risk management).

Among the many available examples, it is worth mentioning the following assessment, the USDA “Pest Risk Assessment for Importation of Solid Wood Packing Materials into the United States” drafted in 20048. The pest risk assessment team selected 19 representative species or groups of

6 “Where appropriate, the provisions of the Convention may be deemed by contracting parties to extend, in addition to plants and plant products, to storage places, packaging, conveyances, containers, soil and any other organism, object or material capable of harbouring or spreading plant pests, particularly where international transportation is involved.”7 PRATIQUE, No. 212459, Deliverable number: 4.6, Date: 25/07/2011, Pathway Risk Analysis Framework including Systems Approach - PD No. 4.6 - Authors: John Mumford, M. Megan Quinlan, Jon Knight, Adrian Leach, John Holt, Richard Baker and Françoise Petter. Partners: Imperial College London, FERA, EPPO, Final version submitted: 25 July 2011. CFR, Baker et al. (2009).

8 https://works.bepress.com/judith_pasek/23/

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insects and fungi of potential concern for detailed assessments to represent an array of geographical origins, host types, and pest habitats. Pest risk potentials were described in relation to current regulations and practices and without regard to potential mitigation measures or proposed regulations (i.e., baseline assessment). Experts evaluated seven risk elements for each potential pest to obtain an overall qualitative ranking (high, moderate, or low pest risk potential). Four of these elements related to likelihood of introduction: (1) pest with host or commodity at origin potential, (2) entry potential, (3) establishment potential, and (4) spread potential. Elements describing consequences of introduction included (5) economic damage potential, (6) environmental damage potential, and (7) social and political considerations.

Control points in P-PRAPathway risk analysis may identify control points along a pathway that may provide opportunities for risk management (NAPPO 2012). Management measures could focus on evaluating the control points associated with pathways or pathway events representing the highest risk and continuing to develop and evaluate measures until an acceptable level of risk has been achieved. Measures may be identified in addition to industry practices or may be adapted or adopted from industry practices alone or in a systems approach. Each control point can be assessed to determine if risk management options can be applied and to estimate the effectiveness of these management options. Where necessary, multiple phytosanitary measures may be applied at one or multiple control points in order to minimize the risk to an acceptable level (NAPPO 2012).

Organism-based pathway risk analysisOrganism-based pathways risk analysis are analyses of pathway(s) that are conducted on a specific pest or alien species but with a relevant focus on one or more pathways (e.g. a fruit fly species). They are a special type of pathway risk analysis as they are species-initiated and might consider more than one commodity or pathways that make use of different vectors that cannot be considered commodities.

As remarked by NAPPO (2012), many NPPOs consider pest risk in relation to the importation of commodities. This is the focus of several of the IPPC’s phytosanitary standards. However, some plant pests or invasive alien species, depending on their biology, do not have to be necessarily associated with a host plant in order to be introduced to a new area. For example, night time flying insects can easily be drawn into cargo containers if they are loaded at night under bright lights (e.g. Caton et al. 2006). Weed seeds may become attached to clothing or get lodged in the intake grills of refrigerated containers or in agricultural machinery. Snails have been known to be intercepted in containers of tiles. Plant pests can also be introduced or spread through pathways not directly associated with trade in plants for planting and plant products. Military equipment and personnel returning from overseas can spread pests if soil and plant debris is not cleaned off equipment. Other means, including railways, roadways, waterways, and other corridors, can act as pathways for the natural or human mediated introduction and spread of pests and invasive alien species both within and between areas (NAPPO 2012).

As reported by Rathé et al. (2015), the “aircraft pathway” for “hitchhiking” insect pests has been investigated both with a focus on interception data (Caton et al. 2006, Liebhold et al. 2006) and experimental testing of the aircraft conditions that insects will be exposed to (Russell 1987). Rathé et al. (2015) have studied the glassy-winged sharpshooter, Homalodisca vitripennis, an insect that transmits the economically important plant pathogen Xylella fastidiosa. This research increased our understanding of the level of risk associated with long-distance air transport as pathway of entry for H. vitripennis into countries currently free of the pest.

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Commodity-based pathway risk analysisCommodity-based pest risk analyses are a special type of pathway risk analyses as they are pathway-initiated and they consider pest risk associated with that pathway (NAPPO 2012), i.e. are focused on analysing the risk of pests entering an area or a country by moving with a specific commodity (Devorshak 2012). Therefore, commodity-based pest risk analyses are usually considered a special type of pathway risk analysis since the pathways are more clearly defined. Furthermore, they may also describe some aspects of the host and pathway that are relevant to pest risk. However, functionally, these analyses are a collection of individual pest risk analyses grouped together based on a single commodity (NAPPO 2012).

For example, Eschen et al. (2017) recently remarked that the volume of the international trade in plants for planting (i.e. ‘Plants intended to remain planted, to be planted or replanted’; FAO 2012 9), which include rooted and unrooted plants, cuttings, bulbs and tissue cultures, has increased strongly in the past decades and so has the annual number of new alien pests recorded in many countries. This is based on several researches, such as Liebhold et al. (2012) and EPPO (2012) 10. In their research these Authors define a “commodity” as a specific combination of one plant taxon and one country of origin (for example Dracaena-Costa Rica). Taking into account that the phytosanitary risk of imported plant material depends on the growth form, intended end-use, known pest associations and the type of imported material, Eschen et al. (2017) propose two main criteria for prioritising high-risk commodities: (1) genus characteristics11, and (2) trading history. According to this methodology, the highest risk category would need immediate risk assessment, because all risk criteria are met: perennial half-grown plants/trees that are destined to be planted outdoors, that belong to genera that include hosts of harmful organisms recommended for regulation by EPPO and that are imported from new trading partners.

Pathway(s) assessment and analysisThere are available methods and existing studies on pathways’ analysis and assessment that are not P-PRA in the narrow sense. In a number of cases, these studies are usually supported by specific data-bases, e.g. data bases on pest/IAS interceptions on vectors commodities and pathways. The available databases are in some cases originated by the collection of interception data, and in other cases are scientific review or meta-analysis on existing data (e.g., Claudi & Ravishankar (2006) on ballast water, Kraus (2007) on Reptiles and Amphibians, Desprez-Loustau et al. (2010) on fungi; Yemshanov et al. (2012) on forest insects; Nentwig (2015) on spiders; Faulkner et al. (2016) on vertebrates, invertebrates and plants; Carpio et al. (2017) on game species).

However, when the outcome of a pathway assessment or analysis is a reduced set of pathways (or vectors) that represent considerable risk and can be managed with reasonable efficacy, there is a similarity of outcomes with a full P-PRA. This set of priority pathways can then be used to determine the allocation of resources and to inform policy and other management tools12. As such, these pathway analyses are often named pathway prioritisation.

9 FAO (2012) International standards for phytosanitary measures no. 5. Glossary of phytosanitary terms. IPPC, Rome. https://www.ippc.int/largefiles/adopted_ISPMs_previousversions/en/ISPM_05_En_2012-05-07(CPM-7).pdf

10 EPPO Study on the Risk of Imports of Plants for Planting, EPPO Technical Document No. 1061, Paris. https://www.eppo.int/media/uploaded_images/RESOURCES/eppo_publications/td_1061_plants_for_planting.pdf

11 According to Eschen et al. (2017) Pest risk usually increases with plant age and size, as older plants have had longer exposure to potential pests and larger plants have a larger diversity of pests. The presence of soil increases the risk of introducing soil organisms. Hence, the different sizes, forms and life stages of imported plants for planting can be classified in order of increasing phytosanitary risk (i.e. in vitro, seeds, cutting, seedling, young plant, half-grown plant, full-grown plant).

12https://www.une.edu.au/__data/assets/pdf_file/0004/20587/Pathway-risk-analysis-for-weed-spread-within-Australia,-Appendix-3.pdf

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Importantly, sentinel tree nursery and sentinel plantings are a very effective early warning system for pathway risk assessment and analysis. As described by Eschen et al. (2017, 2018), sentinel plantings in exporting countries to detect arthropod pests and agents of diseases prior to introduction provide information about the likelihood of introduction and the potential impact on plants native to the importing country. Such plantings can consist of species that are native to exporting or importing countries (“in-patria” and “ex-patria” plantings). In-patria plantings consist of young woody plants of species that are commonly exported and can be used to identify pests that may be introduced to new countries via the trade in live plants. Ex-patria plantings consist of exotic young or mature woody plants and surveys may provide information about potential impacts of pests if these were to become established in a new country.

Also, a first pathway-level economic risk analysis assessing the current scientific evidence for the net benefits of a phytosanitary policy was made by Leung et al. (2014) on the basis of the best available economic and ecological information surrounding International Standards for Phytosanitary Measures No 15 (ISPM15), a pathway-level international phytosanitary policy for treatment of wood packaging material.

Pathway model(s)According to Douma et al. (2016)13, a “pathway model” simulates the movement of propagules or their vectors (carriers) from a source along path with segments that are distinguished by discrete points to one or more points within a geographic area of concern. Pathway models quantify the number of pest propagules that might be moved into an area of concern (hereafter referred to as exposure). Most models can describe the outcome of several scenarios by modifying model inputs or management options, such as effects of changes to inspection, processing and transport, that may affect processes represented within the model”. Douma et al. (2016) used terminology from graph theory to describe pathway models. In pathway models, nodes represent spatial locations or categories of spatial locations relevant to the introduction process of the carrier or the pest. Examples of nodes are import locations, storage and packing houses and nurseries. For example, for the processing of imported logs into lumber, the logs might first arrive at a port of entry (node 1), be moved to a storage area (node 2) and processed at a mill (node3).

Holt et al. (2017) designed a quantitative pathway model, QPAFood, to support risk assessment for plant pest entry into European Union (EU) territory on a range of edible plant commodities via trade flows. The model calculates the distribution of an imported infested/infected commodity along a pathway into and within the EU from source countries, based on Eurostat data and other data/information. The model determines the implications of global trade pathways for the potential arrival of the infested commodity in the EU28 Member States. Within each Member State, the calculation proceeds by distributing the commodity according to uses, notably retail or processing, to the vulnerable area of commercial host crops determined in each NUTS2 region 14 and then quantifies the consequent potential for pest–host contact which could lead to pest transfer. Annual and monthly estimates of contact risk are tabulated and visualized for Member States and NUTS2 regions. The model by Holt et al. (2017) was developed originally for the European Food Safety Authority using four case studies of specific pest-commodity combinations. These pests had relatively limited host ranges and the model has now been extended in the context of the EC FP7 DROPSA project for the multiple commodity pathways associated with the highly polyphagous fruit pest Drosophila suzukii.

13 In this paper the authors follow the definition of pathways by Richardson, D.M., Py šek, P., Carlton, J.T., 2010. A Compendium of Essential Concepts and Terminology in Invasion Ecology, Fifty Years of Invasion Ecology. Wiley-Blackwell, pp. 409–420.

14 Nomenclature of Territorial Units for Statistics, see details here: https://ec.europa.eu/eurostat/web/nuts/background

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Benninga et al. (2012) developed a chain risk model (CRM) to calculate the cost-effectiveness of phytosanitary measures. The CRM is a quantitative model for phytosanitary assessments of all kinds of agricultural product chains. In the CRM, chain stages are connected by the product volume streams at which infections of pests can be spread from one stage to another. The arrangement of the stages in the chain can be varied by the model’s user. Primary infection of a pest in the chain stages can take place by imported commodities, from a former chain stage and from outside. Spread of pests is simulated by a spread factor and the multiplying factor of the product itself, estimated by the model user. The costs of measurements assessed and their effect on the pest or detection of the pest have to be entered in the model. The result of the model calculations is the cost effectiveness of a measurement or set of measurements. An additional result is an overview of the distribution of infected lots in the chain. Experience with the CRM has been gained by applying it to two actual problems: Clavibacter michicanensis subsp. michicanensis, which causes bacterial wilt and canker of tomato (Lycopersicon esculentum L.) and Potato spindle tuber viroid (PSTVd) in potato (Solanum tuberosum L.), which is also called tomato bunchy top virus. Both cases confirm the hypothesis that CRM is applicable for the assessment of various sets of measurements, like checks in different chain stages and application of a quality care system in some stages. The CRM is primarily intended for use by the Dutch Plant Protection Service (nVWA) but can also be used by other national plant protection organizations. The generic and flexible model can be used for calculations on topics as assessment of new detection techniques, assessment of risk reduction measurements on pathways and assessment of different alternatives of sampling in relation to different kinds of phytosanitary checks.

For the risk analysis of the invasion pathway of the Asian gypsy moth, Gray (2017) used the available information regarding the transportation route of the vector (ships), and a phenology model that estimates vector contamination (propagule size), the probability of introduction, and the probability of initial establishment given an introduction. In fact, the probability of an Asian gypsy moth introduction by the investigated stowaway pathway is very strongly seasonally variable. Due to this temporal dependence, Canadian and US regulations employ two tactics at two points in the invasion process: (1) ships that have visited a regulated port during the ‘‘risk period’’ that designates the phenological window of female moth flight and oviposition must undergo a pre-departure inspection and cleaning to receive Asian gypsy moth-free certification; (2) these same ships are subject to further inspection at protected ports if they arrive during the ‘‘risk period’’ of the port.

Assessing and prioritising pathways: the Euphresco project report A recently published Euphresco project report entitled “Assessment and prioritisation of pathways” provides some useful guidance, particularly in relation to the two following objectives:

Develop proposals to overcome existing difficulties in assessing pathways; Provide a report on options for the systematic evaluation and prioritisation of pathways.

Six pathway components for generic plant trade pathways, were identified: four of the pathway components exist in the pre-border space for the importing country or trading bloc (Point of Origin, Production Practices, Post-harvest Treatment, Transport and Storage) one involves the processes on the border at the point of entry into the importing country or trading bloc (Border Process), and the final component (End Use at Destination) represents the post-border processes within the importing country or trading bloc. Knowledge gaps which would need addressing to allow pathways assessments to be more widely performed, along with suggestions for approaches to filling these knowledge gaps, were identified. As a result, it appeared that nearly all options to overcome the difficulties with assessing pathways would require additional resources to those already deployed by countries to undertake inspections).

Ways in which pathways assessments are being approached by different countries varies significantly. There is no current accepted best practice for using pathways assessments to justify restrictions on trade, and this would be a key requirement if a pathways approach were to replace

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the pest specific risk assessments currently used by most countries. The information required for pathways assessment can only be obtained if there is international cooperation. The development of a set of coherent methods for pathways assessment is vital to minimise the burden to countries in obtaining or supplying data for the assessment.

The report also includes an annex with “Options for the systematic evaluation and prioritisation of pathways”, which provides insights in relation to Semi-quantitative assessments, Quantitative pathway analysis, Decision trees, Probabilistic Models, and Multicriteria decision analysis (MCDA) tools.

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OIE Experiences/practices beyond IASSome work of the World Organization for Animal Health (OIE) in relation to IAS is summarized and discussed by Burgiel (2017). As reported by Burgiel (2017), while the OIE ostensibly deals with animal health, its primary focus is on animal diseases, particularly those affecting livestock and animal products involved in international trade. It maintains a list of priority animal viruses and diseases requiring national notification, which includes some diseases with significant potential to impact biodiversity in the wild (such as amphibians, bees and fish). There have been a range of discussions with other international agreements and among member countries about the breadth of the OIE’s mandate, particularly its ability to address invasive alien animals, and not just diseases. While there are legal interpretations to support that view, the limiting factor is a lack of resources and interest among member countries to expand its range of activities that broadly. That said, the OIE has developed guidance on how to conduct risk assessment to evaluate the potential invasiveness of animals.

In particular, guidelines for assessing the risk of non-native animals becoming invasive were developed by the World Organization for Animal Health (OIE 2011). According to this document a risk assessment is to be done to determine whether such imported animal species are likely to become harmful to the environment, animal or human health, or the economy. The “Entry assessment” is the specific step which consists of describing the pathway(s), biological or non-biological, necessary for an importation activity to introduce non-native animal species into a particular environment, and estimating the probability of that complete process occurring, either qualitatively (in words) or quantitatively (as a numerical estimate). The entry assessment describes the probability of the entry of each of the hazards (the non-native animals) under each specified set of conditions with respect to amounts and timing, and how these might change as a result of various actions, events or measures.

The World Organization for Animal Health also published two volumes of a handbook which introduces the concept of import risk analysis and discusses quantitative risk analysis (Murray et al. 2004, Bruckner et al. 2010). This guidance provides practical guidance to veterinary services that are required to analyse the risks posed by imports, to ensure that risks are identified and properly managed, and may also be a useful training guide. The OIE volumes introduce quantitative risk analysis, including deterministic and probabilistic risk assessment, differentiating variability and uncertainty and sampling values from a probability distribution. There are also chapters on probability and probability distributions, theorems providing a basis for probabilistic risk assessment, useful probability distributions, probability processes and calculations, determining a distribution to represent a variable, second order modelling and guidelines for developing a risk assessment model.

According to a review made by Peeler et al. (2015) the OIE model is designed to assess the magnitude of the risk (measured qualitatively or quantitatively) for specified hazards and can be used to decide whether the risk is acceptable or whether sanitary measures are required to reduce it to the acceptable level of risk. Risk analysis is the formal method to deal with hazards and associated risks and has been well documented as a step-by-step process. Hazard identification is the first step and considered separately from the risk assessment. The risk assessment process itself is subdivided into three steps: (i) entry (release) assessment (description of pathways necessary for the introduction of the hazard), (ii) exposure assessment (description of pathways necessary for the hazard to occur following introduction) and (iii) consequence assessment (identification of the consequences of disease introduction and establishment, that is, the adverse human health, animal health, economic or environmental effects of interest). An overall risk estimation is made by integrating the release, exposure and consequence assessments.

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Pathogens in aquaculture

An interesting overview of the risk analysis approach in relation to pathogens in aquaculture, is provided by Bondad-Reantaso and Arthur (2008), according to whom the actual risk assessment consists of four components, strictly related to pathways:1. Release assessment is the step that determines the pathways whereby a pathogen can move

with the commodity from the exporting country to the border of the importing country and the likelihood of this occurring;

2. Exposure assessment is the step that determines the pathways by which susceptible populations in the importing country can be exposed to the pathogen and the likelihood of this occurring (the pathways necessary for exposure of animals and humans to the potential hazards and estimate of the likelihood of exposure);

3. Consequence assessment: impact;4. Risk estimation is the step that calculates the overall risk posed by the hazard (the unmitigated

risk) by combining the likelihood of entry and exposure with the consequences of establishment.

In the risk assessment process, the use of pathway analysis and scenario diagrams is very important. They serve as useful tools in identifying possible routes (pathways) and the individual events or steps in each pathway that need to occur for a given pathway to be successfully completed. Not only do they provide a logical process by which the critical risk steps (events) leading to pathogen introduction and establishment in an importing country can be identified, they also allow estimation of the probability of each event occurring, thus leading to an overall estimate of the probability of a given pathway being completed.

During the pathways scenario portion of the risk assessment process, when sensitivity analysis reveals key information gaps that must be addressed by targeted research, the “precautionary approach” may come into play within the context of risk analysis for aquatic animals.

Also, the document prepared by the Department of Fisheries Western Australia on “Threat Identification, Hazard Pathway Analysis and Assessment of the Key Biosecurity Risks presented by the establishment of the Mid West Aquaculture Development Zone in Western Australia”15 includes some relevant information. In the document potential pathways leading to a pathogen introduction and potential disease outbreak in an MWADZ aquaculture facility (that may lead to potential spread of disease to wild fisheries and subsequent significant impact) are assessed. In particular, the process for assessment included the following components:

- threat identification; - hazard pathway analysis;- identification of overarching risks and their assessment; - overarching risk assessment (including risk management).

The hazard pathway analysis, as the exercise is named, is mostly equivalent to a pathway analysis in the field of biological invasion. In fact, for the purpose of hazard pathway analysis, hazards were considered based on biological consequence to target species, ecosystem and/or habitat. The hazard pathway components were individually analysed with respect to both the inherent hazard (baseline hazard if no management measures to mitigate the hazard were in place) and their residual hazard (remaining hazard once one or more of the proposed management controls have been effected). For each component, the following criteria have to be assessed/scored: 1) Likelihood; 2) Consequence; 3) Hazard score; 4) Risk level.

15 http://www.fish.wa.gov.au/Documents/other/public_comment/appendix_4_-_biosecurity_risk_assessment.pdf

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Closing remarksSeveral experiences exist in the EU and beyond in relation to efforts made to analyse and risk assess pathways with the aim to identify those that should be prioritised. Many other studies are currently underway in view of the reporting required by the EU IAS Regulation by 1 June 2019 (but should be available in the next few months). While most applied methods focus on a simple quantification of pathways (i.e. on terms of volume of IAS and frequency of introductions), others also take into account other elements, particularly the impact of the involved species, the costs and efficiency of the available management options, etc.

Challenges and potentialities of each study are usually discussed in the relevant works, which the readers should refer to. A major constraint that is common across most studies is related to the limited availability of the required information and data on specific pathways. This may be particularly evident in the case of unintentional introductions, which should be the focus of the analyses, as they are mostly aimed at addressing this type of introduction, rather than intentional ones. Overall, the studies carried out are very different among countries and taxonomic group, hence comparisons and trends are difficult to assess. For this reason, a standardized approach taking into account different levels of detail (including in relation to the availability of data, which may be more or less comprehensive), should be envisaged.

Experiences from fields other than invasion biology may be interesting to look at, but the relevant methodologies are difficult to transfer directly to the alien species pathways, because of possible inconsistencies in relation to terminology and purposes of the analyses. While such experiences would definitely benefit a process of standardisation of practices of pathway analysis in the field of biological invasions, it is evident that further research is needed to achieve useful results.

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