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Article

Invasion Potential of Ornamental Terrestrial Gastropods in Europe Based on Climate Matching

by
Lucie Bohatá
and
Jiří Patoka
*
Department of Zoology and Fisheries, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Kamýcká 129, 165 00 Prague, Czech Republic
*
Author to whom correspondence should be addressed.
Diversity 2023, 15(2), 272; https://doi.org/10.3390/d15020272
Submission received: 14 December 2022 / Revised: 9 February 2023 / Accepted: 10 February 2023 / Published: 14 February 2023
(This article belongs to the Collection Feature Papers in Animal Diversity)
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Abstract

:
Invasive species are one of the main causes of biodiversity loss worldwide. Pet trade is a well-known pathway for the introduction of non-native species. Prevention is the most effective, least time-consuming, and least financially demanding way to protect biodiversity against the spreading of invasive species. The main part of prevention is the early detection of a potentially high-risk species, as well as the successful implementation of prevention strategies in legislation and practice. This study summarizes the pre-introduction screening of pet-traded terrestrial gastropod species and their potential occurrence in the EU territory. Based on the list of species traded in the Czech Republic, one of the most important global hubs of the pet trade, 51 species (49 snails and 2 slugs) were analysed. Due to a lack of certain native occurrence data, only 29 species (28 snails and 1 slug) from 10 families were modelled using MaxEnt software. Twenty species from seven families have potential occurrence in the EU territory. Based on MaxEnt modelling, we considered the following species to be high-risk candidates for the EU: Anguispira alternata, A. strongylodes, Laevicaulis alte, Megalobulismus oblongus, Rumina decollata, and R. saharica. Based on this estimation, we present considerations with which to further improve the risk assessment and recommend continuous monitoring of the pet trade market.

1. Introduction

Anthropogenic activities have a substantial influence on biodiversity, as shown in [1,2,3]. Human globalization has overcome natural geographical barriers limiting the spread of organisms, which are removed from their native range in large numbers [4,5,6]. In this, gastropods are not an exception. Even if certain species have only been reported from greenhouses [7,8,9], various terrestrial gastropods (so-called “land snails and slugs”) are classified as invaders or at least potentially invasive species due to their significantly negative impact on native biota and entire ecosystems [6,10,11,12]. Invasive land snails are occupying free niches, out-competing native species, e.g., for food resources or predation on native species, and also serve as hosts and vectors of non-native pathogens [13,14].
Lissachatina fulica (Bowdich, 1822) is an invasive species in many countries worldwide [10,11]. It negatively impacts plant production, the diversity of invertebrates and native plant species, and serves as a vector of parasites and pathogens [15,16]. Another example is Cornu aspersum (Müller, 1774), a species native to the Mediterranean region and Western Europe. In California and Florida, C. aspersum is an agricultural and garden pest causing great socio-environmental losses annually [17].
Irresponsible management practices support biological invasions. For instance, Euglandina rosea (Férussac, 1821), Gonaxis spp. and Rumina decollata (Linnaeus, 1758) were intentionally introduced to control previously introduced pest snails; however, paradoxically, they preyed on native species instead of invasive ones [18,19,20], causing the extinction of several endemic gastropod species in some Pacific islands [6].
Terrestrial gastropods have a relatively low ability for active dispersal [21,22,23]. Over longer distances, they spread through passive dispersal using various vectors [24]. Live gastropods are transported in the digestive tract of their predators such as birds [25,26], by adhesion on the body surface of vertebrates [27], or by attaching to transferred material such as food and nesting material [28,29]. Many examples of the spreading and subsequent establishment of terrestrial gastropods out of their native range are associated with human activities such as the unintentional transport of commodities, agriculture, pet trade, medical reasons, and farming for human consumption [6,11,30,31,32]. Many invasive species have been introduced via different pathways and for various purposes that are poorly studied, such as Arion subfuscus (Draparnaud, 1805), Bradybaena similaris (Férussac, 1822), Deroceras reticulatum (Müller, 1774), Sarasinula plebeia (Fischer, 1868), and Elisolimax flavescens (Keferstein, 1866) [33,34,35,36]. Mostly, the continuously increasing local and international pet trade has been identified as one of the major sources of invasive species worldwide [1,37,38,39,40].
Wittenberg and Cock [41] suggested four basic strategies for handling non-native species: (1) prevention, (2) early detection, (3) eradication, and (4) control. Among these strategies, prevention involves the identification of potential future invaders before their introduction, and early detection and eradication of harmful invasions soon after establishment are often seen as the most effective approaches [42]. The prevention of new introductions is the most successful; moreover, since early detection is difficult, controlling the species can be very expensive, and its total eradication may be impossible in many cases. Even where an optimal non-native species policy involves a combination of all aforementioned strategies [43], the role of prevention is crucial. Prevention integrates environmental modelling and risk assessment, general public education, monitoring of introduction pathways, and the improvement of legislation (e.g., regulation of trade) [44,45]. In the case of environmental modelling, a climate-matching analysis comparing selected environmental parameters such as temperature, moisture, and precipitation between the native range and target area is commonly used [40,46,47].
Even if the prevention of biological invasions is the most important way to protect the environment, the efficiency of supporting restrictions is somewhat controversial because detailed analyses of high-risk species and related risks are lacking in certain cases [48,49]. The European Union (EU), as a party to the Convention on Biological Diversity, regulates the transportation, marketing, keeping, and breeding of invasive species threatening EU countries according to Regulation (EU) 1143/2014 on the prevention and management of the introduction and spread of invasive alien species. The Union List of invasive alien species of EU concern (Commission Implementing Regulation (EU) 2016/1141, 2017/1263 and 2019/1262) currently lists 30 animal species, including crustaceans, fish, amphibians, reptiles, birds, and mammals, as well as 36 plant species. It is obvious that many problematic species have been omitted from this list, such as, for example, the over 250 species of alien mollusc that Hulme [50] claims to be in Europe.
In comparison to aquatic species [51,52,53], the pet trade as an introduction pathway and the market are poorly studied regarding terrestrial gastropods, while related risks are highlighted only sporadically [54]. The Czech Republic is considered one of the leading countries contributing to the global pet trade market. This country is known as a significant importer, exporter, and producer of pet animals for ornamental keeping and as a gateway to Europe [55,56]. For this reason, we decided, based on the surveyed availability of terrestrial gastropod species on the ornamental market in the Czech Republic [57], to analyse their probability to establish new populations in the territory of the EU via climate matching.

2. Materials and Methods

The definition of the term “invasive (alien) species” is not uniform and clear. For the purposes of this analysis, we followed ecological terminology [58]: an invasive species is defined as a non-native species rapidly multiplying and spreading out of its native range with a negative impact on native biota.
The list of traded species (Table 1) was adopted from Bohatá and Patoka [57], and the current taxonomy of each species was adopted from https://www.molluscabase.org/ (accessed on 4 January 2023). Fifty-one species (49 snails and 2 slugs) from 11 families were analysed using climate matching for the European Union territory and the Schengen Area [51] using MaxEnt (v.3.4.1; https://biodiversityinformatics.amnh.org/open_source/maxent, accessed on 5 January 2023) [59]. Pet owners, traders, and breeders usually sort ornamental gastropods according to their “breeding difficulty” (including adaptability, opportunistic feeding, reproduction, etc., according to landsnails.org, https://aquariumbreeder.com/, accessed on 4 January 2023).
Based on previously published information on species native occurrence [11,62], environmental layers including temperature, moisture, and precipitation were selected, and maps showing the potential occurrence of each species were modelled. Available GPS coordinates of native occurrence were obtained from the Global Biodiversity Information Facility (GBIF; https://www.gbif.org, accessed on 5 January 2023), according to published records, e.g., [63], and online databases (ADW https://animaldiversity.org/, Terrestrial Mollusc Tool https://idtools.org/id/mollusc, WMSDB https://www.bagniliggia.it/WMSD/WMSDhome.htm, all accessed on 5 January 2023). Environmental layers were obtained from the CliMond database (v.1.2; https://www.climond.org/, accessed on 5 January 2023) with a spatial resolution of 10 arcmins (∼1 km2). The CliMond datasets were applied for a reliable climate-matching model of invasive species with a suitable spatial precision result [64]. The datasets were assembled in QGIS 3.8.2 Zanzibar (https://qgis.org/en/site/, accessed on 5 January 2023) to ASCII format and used in the MaxEnt algorithm.
MaxEnt is a maximum entropy model that is well suited for species distribution mapping [65,66] and is widely used to predict non-native species’ distribution [67,68]. The final set of environmental predictions included 27 bioclimatic layers (Bio1–Bio19, Bio28–Bio35) (Table 2). For the models, 80% of presence records were randomly selected and used in model training while the remaining 20% were used in model testing. The number of records was different in each evaluated species and was always based on available data from the GBIF database. The model described a continuous probability surface of habitat suitability in the target area of European Union territory. For the cumulative output, a continuous map was generated for each evaluated species and visualised in QGIS 3.8.2 Zanzibar (https://qgis.org/en/site/, accessed on 5 January 2023). According to statistical evaluation of model testing, threshold values for the predicted areas of each species were applied based on balance training omission [65,69,70]. Areas reaching or exceeding the specific threshold were interpreted as areas where there is no evidence of climatic constraints for the survival of the evaluated species (coloured red on the map).
Species threshold values were calculated during the modelling of the predicted potential occurrence maps for each evaluated species (Table 3). The models had a training area under the receiver operator curve (AUC) value of over 0.95 (Table 3), suggesting the high predictability of the model [71]. The AUC value determines the validity of the model and the probability that a random selection from the presence records had a model score greater than a random selection from the absence records [67]. Species threshold values and AUC values for each species are provided in Table 3.
The degree of potential risk was evaluated based on the size of the predicted occurrence of the species: S—a small area was defined according to the prediction of potential occurrence in Macaronesia in the southern part of the evaluated territory of the EU only; M—medium-sized area covering less than 5% of the territory; L—large area covering more than 5% of the territory.

3. Results

Only 29 species out of 51 terrestrial gastropods pet-traded in the Czech Republic (shown in Table 3) were evaluated, as the data were deficient for the rest. Nine of them, i.e., Achatina achatina (Linnaeus, 1758); Achatina schweinfurthi von Martens, 1874; Limicolaria martensiana (Smith 1880); Hemiplecta distincta (Pfeiffer, 1850); Caracolus marginella (Gmelin, 1791); Caracolus sagemon (Beck, 1837); Zachrysia guanensis (Poey, 1858); Z. provisoria (Pfeiffer, 1850); and Subulina octona (Bruguière, 1789), were without predicted potential occurrence in the European Union (EU) territory. According to our results, the remaining 20 species belonging to seven families may potentially occur in the EU. Ten species, i.e., Cochlitoma varicosa (Pfeiffer, 1861); Helicophanta bicingulata (Smith, 1882); Hadra webbi (Pilsbry, 1900); Phaedusa paviei (Morlet, 1893); Anguispira alternata (Say, 1817); Anguispira strongylodes (Pfeiffer, 1855); Megalobulimus oblongus (Müller, 1774); Rumina decollata (Linnaeus, 1758); Rumina saharica (Pallary, 1901); and Laevicaulis alte (Férussac, 1822) were predicted to cover a large area of the EU territory (Figure 1). Four species, i.e., Archachatina marginata (Swainson, 1821); Archachatina ventricosa (Gould, 1850); Acavus superbus (Pfeiffer, 1850); and Lissachatina allisa (Reeve, 1849) were predicted to cover a medium-sized area (Figure 2), and six species, i.e., Achatina balteata (Reeve, 1849); Limicolaria flammea (Müller, 1774); L. aurora (Jay, 1839); Lissachatina fulica (Bowdich, 1822); L. reticulata (Pfeiffer, 1845); and Helicophanta magnifica (Férussac, 1819) were predicted to occupy a small area of the EU (Figure 3).

4. Discussion

Among the 29 evaluated terrestrial gastropod species, 20 species were found to have the potential to establish new populations in the EU territory. This supports the assumption that the pet trade is an important pathway and vector for invasive species [31,48,72,73].
Characteristics of popular pet-traded animals are breeding, handling, and care maintenance based on one or more characteristics such as tolerance to various factors, unspecialised diet, high fecundity, simple rearing, and reproduction modes. Together with climatic characteristics such as temperature and moisture, these properties can be seen as important predictors of the invasive success of evaluated species [12,61]. The best example of this phenomenon is seen for the well-known species (even to the general public) L. fulica [12], which has been introduced in numerous countries worldwide (Global Invasive Species Database GISD ISSG http://www.iucngisd.org, accessed on 5 January 2023). The MaxEnt model used for L. fulica showed the potential distribution of the species in a small area in the EU. This self-fertilizing species is listed among the 100 most invasive species [10] according to its invasion history and significantly negative impacts on biodiversity and economy worldwide. Nielsen et al. [12] classified this species as having moderate risk with an increasing establishment probability due to climate change. Moreover, this species is not the only one from the family Achatinidae expected to have an impact on the biodiversity and economy of many countries [12]. In the USA, the import and interstate transport of all species from the genus Achatina were banned (USDA APHIS https://www.aphis.usda.gov, accessed on 5 January 2023). However, the designation of the genus “Achatina” is misleading because numerous synonyms and misnomers exist (MolluscaBase https://www.molluscabase.org/). Since there are plenty of examples of invasive species being introduced from North America into Europe and vice versa, as shown in [74,75,76], one can conclude that, to these species, the finding of, and acclimation to, available niches and climatic conditions is not a barrier. Therefore, one can assume that the same species may have the potential to invade the same climatic niches in both aforementioned regions.
From the family Discidae, two species are traded as ornamentals: Anguispira alternata and A. strongylodes. According to Nielsen et al. [12], molecular genetic analyses revealed confusing morphological characteristics used in species determination in A. alternata and A. strongylodes. The MaxEnt model confirmed the potential occurrence of both species in a large area in the EU. Although they have a high probability of establishment in Norway, Nielsen et al. [12] determined the risk to be in the medium category given the expected low impact on native biodiversity.
Only one species of the family Strophocheilidae is traded as an ornamental: the predicted potential occurrence of Megalobulimus oblongus was shown in large areas of the EU. In South America, this species is threatened by environmental changes and by non-native species such as L. fulica. The most effective method for controlling L. fulica is manual capture [77]. In addition to the competition, M. oblongus is threatened by this control method due to its confusion with L. fulica [77,78]. If M. oblongus establishes and spreads in a new area, this would be an example of an interesting phenomenon, namely, the so-called “Biodiversity Conservation Paradox” [79,80], when an endangered species, in its native range, behaves as an invader in a non-native range. However, Nielsen et al. [12] classified M. oblongus as a low-risk species.
Rumina decollata and R. saharica from the family Achatinidae are representatives of Palearctic fauna. The medium-sized facultatively self-fertilizing predatory species R. decollata is spreading across the world mainly through the subtropical zone but also in the European temperate zone, negatively affecting native malacofauna [11,12]. R. saharica, a self-fertilizing subtropical predatory snail inhabiting southern Europe, has not yet been confirmed to negatively impact biodiversity; however, the misidentification of R. saharica and R. decollata is possible, while the spread of its native range has been confirmed [12,60]. MaxEnt modelling confirmed the potential occurrence on a large area of the EU for both these species, and Nielsen et al. [12] classified these gastropods as species of moderate risk for R. decollata and low risk for R. saharica.
The occurrence of Paropeas achatinaceum, originally from tropical and subtropical Southeast Asia, has been recorded in the USA [81], in Europe [9], and in Japan (Invasive Species of Japan https://www.nies.go.jp/biodiversity/invasive). Hence, the same pattern of invasion due to similar climate conditions cannot be excluded at least in parts of the EU. Although the MaxEnt model of P. achatinaceum was not evaluated due to a lack of suitable occurrence data, we emphasized that this species is spreading around the world and has obvious invasion potential [12]. Although Hulme [50] lists another representative of this family, Subulina octona, as a potential invasive species in Europe, further references substantiating its occurrence in the European wilderness were not found. Juřičková [7] confirmed the occurrence of this tropical species in Europe, but only in greenhouses and hothouses. Even if Nielsen et al. [12] evaluate this species as low risk in Norway and our MaxEnt modelling has not confirmed a potential occurrence elsewhere in the EU, changing climatic conditions should nevertheless be further monitored.
The American Malacological Society identified members of the family Veronicellidae as taxa with potential major pest significance to the USA, similar to those of the family Achatinidae [61]. Laevicaulis alte and Leidyula sloanii are examples of pet-traded animals with negative impacts on biodiversity, ecosystem functions, agriculture, etc. [12,61]. Laevicaulis alte is self-fertilizing and can lay fertilized eggs multiple times after only a single mating [12]. MaxEnt modelling showed the potential distribution of L. alte in a large area of the EU. Leidyula sloanii was not evaluated due to a lack of occurrence data. From a Norwegian perspective, the occurrence of both of these species was evaluated as potentially possible, even if a low probability was estimated [12].
Tropical and subtropical species without an invasion history on a large area of the EU include Cochlitoma varicosa, Helicophanta bicingulata, Hadra webbi, and Phaedusa paviei. Considering the extent of the area, we recommend their further monitoring and evaluation.
The legislative act focusing on the prevention of new introductions of invasive species in the EU is Regulation No. 1143/2014 and the Union list of invasive alien species. However, the reasons for the species listed and not listed are debatable and not well-defined in certain cases. No gastropods or other molluscs are listed. We have highlighted the seven species identified as high-risk (Anguispira alternata, A. strongylodes, Rumina decollata, R. saharica, Megalobulimus oblongus, Laevicaulis alte, and Lissachatina fulica) for the consideration of policymakers for the next revision of the Union list.
However, sufficient and credible data about many pet-traded terrestrial gastropods are unavailable, partly due to inconsistent taxonomy, overlapping species occurrence, and the difficult determination of subjected species. For these reasons, and due to changing climate conditions and the variation in the adaptability of the found species, we suggest further improving the risk assessment and monitoring of pet-traded animals in general, and for the ornamental terrestrial gastropods in particular. We recommend our findings to the attention of conservationists, wildlife managers, policymakers, and other stakeholders.

Author Contributions

Conceptualization, J.P.; methodology, L.B. and J.P.; validation, J.P.; formal analysis, L.B.; investigation, L.B.; resources, L.B.; data curation, L.B.; writing—original draft preparation, L.B.; writing—review and editing, J.P.; visualization, L.B.; supervision, J.P.; project administration, J.P.; funding acquisition, J.P. All authors have read and agreed to the published version of the manuscript.

Funding

J.P. was funded by the Technology Agency of the Czech Republic within the project “Div Land”, grant number SS02030018 and the European Regional Development Fund (No. CZ.02.1.01/0.0/16_091/0000845).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

We thank four anonymous reviewers for their effort and time when constructively commented and evaluated our manuscript. The English was proofread by Julian D. Reynolds.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. The prediction computed using the MaxEnt model of the pet-traded gastropods with potential occurrence in a “large area” of EU (= covered more than 5% of the territory). The maps show native range in blue and suitability in red, representing a high probability of establishment for these species: (1) Anguispira alternata, (2) A. strongylodes, (3) Cochlitoma varicosa, (4) Hadra webbi, (5) Helicophanta bicingulata, (6) Laevicaulis altea, (7) Megalobulimus oblongus, (8) Phaedusa paviei, (9) Rumina decollata, and (10) R. saharica; (11) map of European Union.
Figure 1. The prediction computed using the MaxEnt model of the pet-traded gastropods with potential occurrence in a “large area” of EU (= covered more than 5% of the territory). The maps show native range in blue and suitability in red, representing a high probability of establishment for these species: (1) Anguispira alternata, (2) A. strongylodes, (3) Cochlitoma varicosa, (4) Hadra webbi, (5) Helicophanta bicingulata, (6) Laevicaulis altea, (7) Megalobulimus oblongus, (8) Phaedusa paviei, (9) Rumina decollata, and (10) R. saharica; (11) map of European Union.
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Figure 2. The prediction computed using the MaxEnt model of the pet-traded gastropods with potential occurrence in a “medium area” of EU (= covering less than 5% of the territory). The maps show suitability in red, representing a high probability of establishment for these species: (1) Acavus superbus, (2) Archachalina ventricosa, (3) A. marginata, and (4) Lissachatina allisa; (5) map of European Union.
Figure 2. The prediction computed using the MaxEnt model of the pet-traded gastropods with potential occurrence in a “medium area” of EU (= covering less than 5% of the territory). The maps show suitability in red, representing a high probability of establishment for these species: (1) Acavus superbus, (2) Archachalina ventricosa, (3) A. marginata, and (4) Lissachatina allisa; (5) map of European Union.
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Figure 3. The prediction computed using the MaxEnt model of the pet-traded gastropods with potential occurrence in a “small area” of EU (= covering only Macaronesia in the southern part of the territory). The maps show suitability in red, representing a high probability of establishment for these species: (1) Achatina balteata, (2) Helicophanta magnifica, (3) Limicolaria aurora, (4) L. flammea, (5) Lissachatina fulica, and (6) L. reticulata; (7) map of European Union and Macaronesia belonging to the EU.
Figure 3. The prediction computed using the MaxEnt model of the pet-traded gastropods with potential occurrence in a “small area” of EU (= covering only Macaronesia in the southern part of the territory). The maps show suitability in red, representing a high probability of establishment for these species: (1) Achatina balteata, (2) Helicophanta magnifica, (3) Limicolaria aurora, (4) L. flammea, (5) Lissachatina fulica, and (6) L. reticulata; (7) map of European Union and Macaronesia belonging to the EU.
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Table
Table 1. The list of pet-traded terrestrial gastropods, species description, family, breeding difficulty (easy, medium, hard, following landsnails.org), native geographic distribution (AT—Afrotropical, AU—Australasian, NA—Nearctic, NT—Neotropical, OL—Oriental, PA—Palaearctic), status (x—no records found, I—invasive, alien, MI—misidentification with invasive species, NN—non-native, P—pest); the source is indicated by upper index letters: a https://www.aphis.usda.gov, b http://www.iucngisd.org, c https://doi.org/10.1093/mollus/eyy062, d https://idtools.org/id/mollusc, e https://www.cabidigitallibrary.org, f https://explorer.natureserve.org (all accessed on 5 January 2023).
Table 1. The list of pet-traded terrestrial gastropods, species description, family, breeding difficulty (easy, medium, hard, following landsnails.org), native geographic distribution (AT—Afrotropical, AU—Australasian, NA—Nearctic, NT—Neotropical, OL—Oriental, PA—Palaearctic), status (x—no records found, I—invasive, alien, MI—misidentification with invasive species, NN—non-native, P—pest); the source is indicated by upper index letters: a https://www.aphis.usda.gov, b http://www.iucngisd.org, c https://doi.org/10.1093/mollus/eyy062, d https://idtools.org/id/mollusc, e https://www.cabidigitallibrary.org, f https://explorer.natureserve.org (all accessed on 5 January 2023).
SpeciesAuthorFamilyBreeding DifficultyNative
Geographic Distribution		Status
Acavus haemastoma(Linnaeus, 1758)AcavidaemediumOLx
Acavus superbus(Pfeiffer, 1850)AcavidaemediumOLx
Helicophanta bicingulata(Smith, 1882)AcavidaemediumATx
Helicophanta magnificaFérussac, 1819AcavidaemediumATx
Oligospira waltoni(Reeve, 1842)AcavidaemediumOLx
Achatina achatina(Linnaeus, 1758)AchatinidaeeasyATP a
Achatina balteata(Reeve, 1849)AchatinidaeeasyATP a
Achatina craveni(Smith, 1881)AchatinidaeeasyATP a
Achatina schweinfurthi(von Martens, 1874)AchatinidaemediumATP a
Achatina tincta(Reeve, 1849)AchatinidaeeasyATP a
Achatina weynsi(Dautzenberg, 1900)AchatinidaeeasyATP a
Archachatina degneri(Bequaert and Clench, 1936)AchatinidaeeasyATP a
Archachatina marginata(Swainson, 1821)AchatinidaeeasyATP a
Archachatina papyracea(Pfeiffer, 1845)Achatinidae-ATP a
Archachatina purpurea(Gmelin, 1790)AchatinidaeeasyATP a
Archachatina puylaerti(Mead, 1998)AchatinidaeeasyATP a
Archachatina rhodostoma(Philippi, 1849)AchatinidaeeasyATP a
Archachatina ventricosa(Gould, 1850)Achatinidae-ATP a
Ceras dautzenbergi(Dupuis and Putzeys, 1901)AchatinidaeeasyATx
Cochlitoma varicosa(Pfeiffer, 1861)Achatinidae-ATP a
Limicolaria aurora(Jay, 1839)AchatinidaeeasyATP a
Limicolaria flammea(Müller, 1774)AchatinidaeeasyATP a
Limicolaria martensiana(Smith, 1880)AchatinidaeeasyATP a
Lissachatina albopicta(Smith, 1878)AchatinidaeeasyATP a
Lissachatina allisa(Reeve, 1849)AchatinidaeeasyATP a
Lissachatina fulica(Bowdich, 1822)AchatinidaeeasyATI b
Lissachatina immaculata(Lamarck, 1822)AchatinidaeeasyATP a
Lissachatina reticulata(Pfeiffer, 1845)AchatinidaeeasyATP a
Lissachatina zanzibarica(Bourguignat, 1879)AchatinidaeeasyATP a
Paropeas achatinaceum(Pfeiffer, 1846)AchatinidaeeasyOLNN f
Pseudachatina downesii(Sowerby I, 1838)AchatinidaehardATP a
Rumina decollata(Linnaeus, 1758)AchatinidaeeasyPAI a
Rumina saharica(Pallary, 1901)AchatinidaeeasyPAMI, NN [12,60]
Subulina octona(Bruguière, 1789)AchatinidaeeasyNTNN [7]
Ariophanta exilis(Müller, 1774)AirophantidaeeasyOLx
Hemiplecta distincta(Pfeiffer, 1850)AirophantidaemediumOLx
Macrochlamys amboinensis(von Martens, 1864)AirophantidaeeasyOLNN c
Hadra webbi(Pilsbry, 1900)CamaenidaeeasyAUx
Oospira vanbuensis(Bavay and Dautzenberg, 1899)ClausiliidaeeasyOLx
Phaedusa paviei(Morlet, 1893)ClausiliidaeeasyOLx
Anguispira alternata(Say, 1817)DiscidaeeasyNAx
Anguispira strongylodes(Pfeiffer, 1855)DiscidaeeasyNAx
Pleurodonte isabella(Férussac, 1822)PleurodontidaeeasyNTx
Caracolus excellens(Pfeiffer, 1853)SolaropsidaeeasyNTx
Caracolus marginella(Gmelin, 1791)SolaropsidaeeasyNTx
Caracolus sagemon(Beck, 1837)SolaropsidaeeasyNTx
Megalobulimus oblongus(Müller, 1774)Strophocheilidae -NTNN d
Laevicaulis alte(Férussac, 1822)VeronicellidaeeasyATI [12,61]
Leidyula sloanii(Cuvier, 1816)VeronicellidaeeasyNTP e, NN f
Zachrysia guanensis(Poey, 1858)Zachrysiidae mediumNTP d
Zachrysia provisoria(Pfeiffer, 1858)Zachrysiidae -NTI e
Table
Table 2. Bioclimatic layers and the contributing variables used in their calculation (https://www.climond.org/, accessed on 5 January 2023).
Table 2. Bioclimatic layers and the contributing variables used in their calculation (https://www.climond.org/, accessed on 5 January 2023).
NumberVariableMinimum Temp (°C)Maximum Temp (°C)Rainfall
(mm month−1)		Pan
Evaporation (mm d−1)
Bio01Annual mean temperature (°C)××
Bio02Mean diurnal temperature range (mean (period max–min)) (°C)××
Bio03Isothermality (Bio02 ÷ Bio07)××
Bio04Temperature seasonality (C of V)××
Bio05Max temperature of warmest week (°C) ×
Bio06Min temperature of coldest week (°C)×
Bio07Temperature annual range
(Bio05–Bio06) (°C)		××
Bio08Mean temperature of wettest
quarter (°C)		×××
Bio09Mean temperature of driest quarter (°C)×××
Bio10Mean temperature of warmest quarter (°C)××
Bio11Mean temperature of coldest
quarter (°C)		××
Bio12Annual precipitation (mm) ×
Bio13Precipitation of wettest week (mm) ×
Bio14Precipitation of driest week (mm) ×
Bio15Precipitation seasonality (C of V) ×
Bio16Precipitation of wettest quarter (mm) ×
Bio17Precipitation of driest quarter (mm) ×
Bio18Precipitation of warmest quarter (mm)×××
Bio19Precipitation of coldest quarter (mm)×××
Bio28Annual mean moisture index ××
Bio29Highest weekly moisture index ××
Bio30Lowest weekly moisture index ××
Bio31Moisture index seasonality (C of V) ××
Bio32Mean moisture index of wettest quarter ××
Bio33Mean moisture index of driest
quarter		 ××
Bio34Mean moisture index of warmest quarter××××
Bio35Mean moisture index of coldest quarter××××
Table
Table 3. The risk results for 29 species evaluated using MaxEnt. The climate matching (CM) for these bioclimatic layers (Bio1–Bio19, Bio28–Bio35) (Sup. 1) is based on the size of the predicted occurrence of the species: S—small area is defined by prediction of potential occurrence in Macaronesia in the southern part of the evaluated territory of the EU only; M—medium-sized area covering less than 5% of the territory; L—large area covering more than 5% of the territory; N—no risk. Species threshold values (the lowest probability value that is the minimum value for suitable habitat) were calculated during the modelling of predicted potential occurrence maps for each evaluated species. The models had a training AUC value over 0.95, suggesting high prediction accuracy.
Table 3. The risk results for 29 species evaluated using MaxEnt. The climate matching (CM) for these bioclimatic layers (Bio1–Bio19, Bio28–Bio35) (Sup. 1) is based on the size of the predicted occurrence of the species: S—small area is defined by prediction of potential occurrence in Macaronesia in the southern part of the evaluated territory of the EU only; M—medium-sized area covering less than 5% of the territory; L—large area covering more than 5% of the territory; N—no risk. Species threshold values (the lowest probability value that is the minimum value for suitable habitat) were calculated during the modelling of predicted potential occurrence maps for each evaluated species. The models had a training AUC value over 0.95, suggesting high prediction accuracy.
SpeciesFamilyCM
(1–19, 28–35)		ThresholdAUC
Balance
CM
(1–19, 28–35)		CM
(1–19, 28–35)
Acavus superbusAcavidaeM0.7570.994
Helicophanta
bicingulata		AcavidaeL1.1680.998
Helicophanta
magnifica		AcavidaeS1.7700.997
Achatina achatinaAchatinidaeN1.2260.997
Achatina balteataAchatinidaeS3.1300.976
Achatina schweinfurthiAchatinidaeN0.7710.985
Archachatina
marginata		AchatinidaeM1.0940.993
Archachatina
ventricosa		AchatinidaeM2.3720.999
Cochlitoma varicosaAchatinidaeL1.7510.998
Limicolaria flammeaAchatinidaeS2.1640.963
Limicolaria auroraAchatinidaeS2.1180.988
Limicolaria martensianaAchatinidaeN1.6090.993
Lissachatina allisaAchatinidaeM2.1770.988
Lissachatina fulicaAchatinidaeS1.1960.997
Lissachatina reticulataAchatinidaeS1.6330.995
Rumina decollataAchatinidaeL1.6940.982
Rumina saharicaAchatinidaeL2.1280.997
Subulina octonaAchatinidaeN0.6110.999
Hemiplecta distinctaAirophantidaeN0.9370.998
Hadra webbiCamaenidaeL1.0680.990
Phaedusa pavieiClausiliidaeL3.3370.998
Anguispira alternataDiscidaeL1.4220.955
Anguispira strongylodesDiscidaeL1.3580.995
Caracolus marginellaSolaropsidaeN0.6170.999
Caracolus sagemonSolaropsidaeN0.9680.998
Megalobulimus oblongusStrophocheilidae L2.7220.980
Laevicaulis alteVeronicellidaeL3.8060.98
Zachrysia guanensisZachrysiidae N0.9930.999
Zachrysia provisoriaZachrysiidae N1.0660.999
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Bohatá, L.; Patoka, J. Invasion Potential of Ornamental Terrestrial Gastropods in Europe Based on Climate Matching. Diversity 2023, 15, 272. https://doi.org/10.3390/d15020272

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Bohatá L, Patoka J. Invasion Potential of Ornamental Terrestrial Gastropods in Europe Based on Climate Matching. Diversity. 2023; 15(2):272. https://doi.org/10.3390/d15020272

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Bohatá, Lucie, and Jiří Patoka. 2023. "Invasion Potential of Ornamental Terrestrial Gastropods in Europe Based on Climate Matching" Diversity 15, no. 2: 272. https://doi.org/10.3390/d15020272

APA Style

Bohatá, L., & Patoka, J. (2023). Invasion Potential of Ornamental Terrestrial Gastropods in Europe Based on Climate Matching. Diversity, 15(2), 272. https://doi.org/10.3390/d15020272

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