The European Union (EU) has recently adopted a regulation on invasive alien species that foresees the possibility of developing lists of species of National Concern. We developed a prioritisation process for alien mammals already established in Italy, but not yet included in the EU list (n = 6 species) and a systematic horizon-scanning procedure to obtain ranked lists for those species that are already introduced worldwide or traded in Italy (n = 213). Experts were asked to score these species, by evaluating their likelihood of establishment and spread and the magnitude of their potential impacts on biodiversity, economy, human-health and society. The manageability of each species was also evaluated, both for the proritisation and the horizon-scanning processes. We produced five lists that ranked species according to their potential spread and impacts and their manageability. These will allow policy-makers to select outputs according to a balance between risk assessment and risk management, establishing priorities for alien species management at the national level.

Biodiversity, horizon scanning, human well-being, impact, Mammalia, non-native species, prioritisation

Establishing a proactive strategy on invasive alien species – i.e. species that are non-native to an area and which may cause environmental or economic harm or adversely affect human health – requires a clear focus on prevention (Simpson et al. 2009). Avoiding the establishment of new species or their spread over large areas greatly reduces the risk that they become invasive (Finnoff et al. 2007). Effective prevention strategies require the identification of those species which are not yet present in a country, but which are likely to enter in the short-medium period, through active pathways (Simpson et al. 2009). This can be done through horizon-scanning protocols. On the other hand, those species which already established could be prioritised for management, through rapid eradication, spatial containment or population control, according to their present spread and manageability.

In 2014, the European Union adopted a regulation (EU Regulation 1143/2014) on the prevention and management of the introduction and spread of invasive alien species. The regulation is based on a list of ‘Invasive Alien Species of Union Concern’ (hereinafter, Union list), identified through a detailed risk assessment (Roy et al. 2017) evaluated by a Scientific Forum and a Committee with representatives of all Member States. To be included in the list, species have to meet a number of criteria: first, to be alien to the territory of the European Union (excluding the outermost regions); second, to have been assessed as invasive or potentially invasive through a risk assessment. Species included in this list are subject to strict provisions for preventing their introduction into the European Union. The regulation includes a ban on import, trade, breeding, release into the environment and the obligation to produce management plans for already established species (Genovesi et al. 2014). The Union list was based on available risk assessments compliant with the minimum standards (Roy et al. 2017), but subsequently, a horizon-scanning approach was used to rank species to be subjected to risk assessment (Roy et al. 2015).

Horizon scanning is a systematic process aimed at identifying emerging issues which may represent threats or opportunities to society (Sutherland and Woodroof 2009). In the field of biological invasion, horizon scanning allows for the rapid screening of a large number of species through expert opinion and consensus method (Sutherland et al. 2011). This procedure has already been successfully applied to rank species according to their likelihood of arrival, establishment and impacts (e.g. Roy et al. 2014; Gallardo et al. 2016). In the UK, horizon scanning was able to correctly identify some alien species that subsequently invaded the country, such as Dreissena rostriformis or Vespa velutina (Aldridge et al. 2014; Roy et al. 2014; Budge et al. 2017). Horizon scanning can thus produce dynamic lists of potential invasive alien species that can be prioritised in regulations.

Within the framework of this EU Regulation, Member states may establish a list of Invasive Alien Species of National Concern, to which provisions and restrictions foreseen for the species of Union Concern may be applied at the national level. Species could be included in national lists only after the evaluation of the same risk assessment procedure used for evaluating species at the EU level (Roy et al. 2017). In 2018, a national legislative decree (no. 230/2017), aimed to adapt national law to EU Regulation 1143/14, entered into force in Italy. The decree provides for the adoption of a national list of invasive or potentially invasive species with the same provisions and restriction foreseen for the Union list.

As a contribution to the development of such a list, the Italian Mammal Society (Associazione Teriologica Italiana: www.mammiferi.org) gathered a group of experts to draw up a proposal for a list of alien mammal species of national concern. This activity was part of a larger initiative promoted by the national Institute for Environmental Protection and Research (ISPRA, identified in the national decree as the governmental agency that technically supports the Ministry of Environment in the application of the EU Regulation at the national level) which addressed the use of a standardised protocol for the assessment many different taxa (e.g. other vertebrates, invertebrates and plants, from terrestrial, freshwater and marine organisms).

Experts tasks: i) carry out the horizon scanning to identify species not yet present in Italy, which could potentially enter, establish, spread and produce impacts in the country and ii) prioritise the management of alien species already present in the country. The horizon-scanning and prioritisation initiatives were based on the analysis of the invasion process and on the resulting unified framework proposed by Blackburn et al. (2011). The framework breaks down the invasion process into a series of stages (arrival in a new area, introduction, establishment and spread), each one characterised by barriers that need to be overcome by individuals, in order to reach the subsequent stage. Additionally, we also considered the impacts that a species could potentially produce on biodiversity, economy, society and human health.

A comprehensive framework for risk analysis encompasses evaluations regarding both risk assessment and options for management of species (Booy et al. 2017; Kumschick et al. 2020b). Risk assessment evaluates the species based on the likelihood of their successful establishment and spread over large areas, and according to the magnitude of their potential impacts over biodiversity or human well-being. Risk management, on the other hand, accounts for the level of manageability of the species, in terms of the effectiveness of prevention measures and the feasibility of their rapid eradication or control. For instance, species that are difficult to eradicate must be considered a priority for prevention (e.g. through trade restriction), while easy-to-manage species could still be eradicated or controlled after establishment.

Our approach was to develop a support system to help policy-makers establishing national priorities. We thus produced different lists highlighting alien species with a higher likelihood of arrival, establish and spread and that could produce negative impacts on biodiversity or human well-being as a consequence of invasion. These evaluations were then integrated with species manageability.

Horizon scanning, aimed at producing lists of potentially invasive alien species, was based on: i) their likelihood of establishing viable alien populations if imported and released in Italy, ii) their potential to impact biodiversity and human well-being and iii) their level of manageability, so as to prioritise species for prevention or management. For species already present in the country, the prioritisation process was carried out mainly to rank them for management purposes (Nentwig et al. 2010; Booy et al. 2017). Both processes followed a structured approach that involved five steps (Gallardo et al. 2016; Matthews et al. 2017).

Step 5: Prioritised lists of non-native mammals

From the final database, we compiled five prioritised lists of mammal species, based on their potential impacts on biodiversity and human well-being. Impacts were evaluated first separately and then together and we also assigned a manageability score, reflecting the possibility to effectively manage the species. For the horizon scanning, we first calculated a score for the likelihood of arrival and spread as follows (Fig. 1):

– SPREAD score = likelihood of arrival in Italy or escape from captivity if already present × likelihood of establishment × [(likelihood of natural spread + likelihood of human assisted spread)/2] (maximum value = 125);

– BIODIVERSITY score = SPREAD score × potential impact on biodiversity (maximum value = 625);

– WELL-BEING score = SPREAD score × [(potential impact on economy + potential impact on human health + potential impact on social aspects scores)/3] (maximum value = 1875).

Figure 1.

Scores used to produce priority lists from horizon scanning and information on probabilities used to calculate them.

The SPREAD score considered that, at the beginning of the invasion process, a species needs to overcome some natural or artificial barriers, to arrive in Italy and spread and that barriers, like those imposed in captivity (e.g. a fence or a cage) might be effective at preventing a species from becoming an invader (Blackburn et al. 2014). The BIODIVERSITY and WELL-BEING scores considering both the likelihood of spread and the potential of impacts are actually risk scores.

We then combined the three scores into an OVERALL IMPACTS score of the likelihood of impacts. In accordance with EU Regulation, the overall score was calculated with a formula that assigned a higher weight to impacts on biodiversity:

– OVERALL IMPACTS score = SPREAD score × [potential impact on biodiversity + (potential impact on economy + potential impact on human health + potential impact on social aspects scores)/6)] (maximum value = 937.5).

An effective strategy aiming at mitigating the impact caused by alien species should consider both the likelihood of prevention and the feasibility and effectiveness of management, once species are established. For this reason, experts were asked to evaluate the manageability of the various species, according to the effectiveness of available prevention measures, including intentional imports and trade regulation, practicality of carrier treatment and the effectiveness of control measures, as well as ease of species recognition in the field. A final score, which considered the likelihood of impacts, feasibility of prevention and effectiveness of control measures was calculated as:

– IMPACT + MANAGEABILITY score = OVERALL IMPACTS score × effectiveness of prevention measures × (effectiveness of control measures/2) (maximum value = 11718.75),

with an emphasis on prevention rather than control. A TOTAL RANK was then calculated for each species as the sum of ranks in the previous lists.

For the prioritisation of those species that were already present in Italy, scores were similar (Fig. 2), except for the SPREAD score, which did not include the likelihood of arrival or escape and for IMPACT + MANAGEABILITY score which was calculated as:

– IMPACT + MANAGEABILITY score = OVERALL IMPACT score [((effectiveness of control measures + current eradication feasibility + eradication potential cost + side effects of the eradication + social acceptability of eradication)/5)].

Figure 2.

Scores used to produce priority lists from prioritisation and information on probabilities used to calculate them.

Addressing the threats posed by species introductions requires a set of interventions aimed at preventing the arrival of new species and controlling those which are already established. In this study, we prioritised those alien mammal species which are already established in Italy and we used a horizon-scanning approach to highlight the potential risk posed by those species that may arrive or escape captivity in the future.

The prioritisation process ranked S. floridanus as the most impacting and easiest to manage alien mammal in Italy. Sylvilagus floridanus is an American cottontail introduced in Italy in the 1960s for hunting, which has indirect detrimental effect on native hares through apparent competition mediated by the predator Vulpes vulpes (Cerri et al. 2017). The second ranked species was the still localised sika deer Cervus nippon, which hybridises with the native red deer Cervus elaphus (Smith et al. 2018), followed by the rapidly spreading Finlayson’s squirrel Callosciurus finlaysonii (Ancillotto et al. 2018). Notably, four out of 11 (36%) mammal species already listed in the Union list are squirrels. In fact, many squirrel species are highly invasive in Europe (Bertolino 2009; Di Febbraro et al. 2016, 2019) and the Eastern grey squirrel (Sciurus carolinesis) is replacing the native Eurasian red squirrel (Sciurus vulgaris) in many countries (Bertolino 2008).

Three species, Sylvilagus floridanus, Cervus nippon and Callosciurus finlaysonii were considered a priority for management actions and, possibly, eradication. However, at present only Sylvilagus floridanus is irregularly subjected to culling programmes in some areas, besides being a huntable species. Cervus nippon and Callosciurus finlaysonii are not managed at all, despite their potential impacts on native species and their relatively limited spatial distribution, which would enable successful management actions (Ancillotto et al. 2018; Loy et al. 2019). This denotes a lack of rapid reaction and the need to raise the awareness about the social and ecological impacts that these and other alien species can cause.

As specified in the Methods section, this study does not deal with well-known invasive species, such as rats and mice (e.g. see Capizzi et al. 2014), only for reasons related to the time of their introduction. However, these species can be of great management importance, often higher than most of those listed here and their lack of inclusion in this work does not imply the lack of motivation for their control or eradication.

Horizon scanning for potential alien species traditionally produces a final overall list of prioritised species (e.g. Roy et al. 2014, 2015). In this work, we produced five distinct lists and a final overall ranking, related to the likelihood of adaptation to local landscape and spread, to impacts on biodiversity and human well-being, alone or synergistically, and the feasibility of preventing the introductions and/or to control populations eventually established. These lists could be used to prioritise species for prevention measures, because they are likely to establish and spread over large areas if arriving in Italy, producing relevant impact on biodiversity and human well-being. A strategy aimed at prevention or, at least, rapid removal after introduction, should be particularly in place for those species that are considered difficult to manage, because controlling their populations, once established and widespread, would not be feasible.

The TOTAL rank could be used to produce a final list, giving priority to species with the highest values in every partial assessment. At the national level, our assessment will be joined in a process involving the inclusion of assessments for other taxonomic groups, such as other vertebrates, invertebrates and plants, both marine and terrestrial. During the evaluations, experts from different taxonomic groups met in a couple of workshops where the scoring system was discussed in order to use the same scale of reference, for example, when assessing the possibility to eradicate a species, the score was given considering also species from other taxa as comparison. Merging different lists in a unified one is a still an ongoing process; however, the scoring methodology presented here will be applied to all taxa to produce a dynamic list which will include species-specific assessments of spread, impacts and manageability.

The resulting list will assist policy-makers in developing a sound list of alien species of national concern. Such a process will likely lead to the production of a final ranking, based on consensus building between experts and policy-makers, who could assign different weights to the various aspects of the invasion process. Our ranking system highlighted those species characterised by a higher likelihood to overcome different barriers through the invasion process (Blackburn et al. 2011), capable of spreading across large areas and likely to produce negative impacts on species and ecosystems or on human well-being, as well as more likely to be difficult to manage.

The EU Regulation on invasive species was specifically adopted to mitigate the impact of alien species on biodiversity (Genovesi et al. 2014). For this reason, when producing the OVERALL IMPACTS score, we weighted more impacts on biodiversity than on human activities. However, our scoring system could be easily adapted to alternative evaluations. For instance, impacts on human activities or the possibility to carry zoonoses may be considered relevant for prioritising the management of alien species. By including the likelihood of spread in calculating the impacts, we also prioritised species that will likely produce a lower impact over larger areas compared to others that will probably have higher impacts, but with a low risk of spread. The reasons behind this choice lies in the easier mitigation of high impacts, through control or eradication when species are still distributed over a restricted area, compared to the mitigation of lower impacts occurring across a vast geographical scale (Panzacchi et al. 2007; Robertson et al. 2017).

Finally, we also produced a list that considers the OVERALL IMPACTS score of a species and the feasibility of its management (IMPACTS score + MANAGEABILITY score), giving more weight to prevention compared to the possibility of control. It is now recognised that an integrated and hierarchical management strategy should act at the different stages of the invasion process, with an emphasis on prevention. The identification of main pathways allows us to prevent many species from entering recipient areas, while control and eradication is generally costly and should be species-specific (Panzacchi et al. 2007; Robertson et al. 2017).

The main pathways of introduction for the mammal species considered in this study are the escape from zoos and from private keepers, followed by intentional releases. This is in accordance with the pathways identified by Genovesi et al. (2009) for mammals already established in Europe. These authors reported that the most frequent pathways for mammal introductions were escapes from fur farms and zoos, intentional releases of animals from captivity and introductions for hunting. However, increasing security systems to captive animals and discouraging hunters from releasing alien mammals have reduced the importance of these pathways, while the release or escape of animals from the pet trade is increasing (Genovesi et al. 2009). In fact, amongst species already established in Italy and here considered for prioritisation, one third have been introduced for hunting (e.g. S. floridanus, A. lervia), but recently the escape or release of animals from captivity prevailed (e.g. C. finlaysonii, C. nippon).

Species included in the list of alien species of National Concern might be subject to strict regulation, which includes a ban on import, trade, possession and release (Genovesi et al. 2014). Therefore, we consider that prevention could be an efficient strategy for most of the evaluated species. However, since only a few mammals will probably be included in such a national list, other actions, such as the adoption of voluntary codes of conducts or guidelines for zoos (Scalera et al. 2012), pet trade (Davenport and Collins 2011) and hunting (Monaco et al. 2016), should be encouraged.

ICAT Schemes are two evidence-based classification systems for evaluating the ecological and socioeconomic impacts of non-native species (Blackburn et al. 2014; Bacher et al. 2017). Their assessment requires the collection and evaluation of all the papers reporting data on impacts produced by the target species in its global introduction range and their scoring according to different mechanisms of impact (Volery et al., 2020). Due to the high number of species to assess, we used an expert-based approach where single experts used ICAT Schemes as reference systems for scoring the species after a rapid search of literature and without considering the mechanism of impact. There is the perception that expert-based evaluations overestimate impacts produced by alien species. When mammals are scored worldwide for ICAT Schemes, a comparison with our assessments could be made.

Our work combined a prioritisation process of mammal species already established in Italy and not listed in the EU Regulation 1143/2014, with a horizon scanning of species traded in Italy or recorded as introduced worldwide. This resulted into ranked lists of species, based on their spread capabilities, their potential impacts on biodiversity and human well-being and the feasibility of their management. All these lists could be used to prioritise mammal species for prevention, banning their trade in Italy or for management. The developed database will be integrated with others produced through horizon scanning for invertebrates, vertebrates, plants, marine and terrestrial and will be used to produce a proposal for a list of Invasive Alien Species of National Concern (art. 12, EU Regulation 1143/2014).

In our evaluation, we chose not to consider those species with a low potential of impact on biodiversity (i.e. with a score = 1) and we also calculated the OVERALL IMPACTS score giving a higher weight to potential impacts on biodiversity with respect to potential impacts on economy, human health or on social aspects. This choice was justified by the focus of EU Regulation 1143/2014 on prevention, mitigation and minimisation of adverse impact on biodiversity caused by alien species and the provision to produce a list of ‘Invasive Alien Species of National Concern’ in accordance with the Regulation. The impacts on human health and the economy were then considered as a secondary aspect. However, the procedure developed in this study could be used as a blueprint for similar prioritisation initiatives (cf. Ziller et al. 2020), as the formulae could be adapted to produce one or more lists of species according to different priorities established by country regulations or policies.

The work of the expert group from the Italian Mammal Society (Associazione Teriologica Italiana: www.mammiferi.org) was promoted by the Institute for Environmental Protection and Research (ISPRA) and funded by the Ministry of Environment and by the LIFE15 GIE/IT/001039 ASAP project.

This paper emerged from a workshop on ‘Frameworks used in Invasion Science’ hosted by the DSI-NRF Centre of Excellence for Invasion Biology in Stellenbosch, South Africa, 11–13 November 2019, that was supported by the National Research Foundation of South Africa and Stellenbosch University.

We are grateful for the suggestions received by Sabrina Kumschick, Helen Roy, and an anonymous referee.