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Open AccessArticle

Potential Invasion Risk of Pet Traded Lizards, Snakes, Crocodiles, and Tuatara in the EU on the Basis of a Risk Assessment Model (RAM) and Aquatic Species Invasiveness Screening Kit (AS-ISK)

Department of Zoology and Fisheries, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Kamýcká 129, Praha 6 - Suchdol 165 21, Prague, Czech Republic
*
Author to whom correspondence should be addressed.
Diversity 2019, 11(9), 164; https://doi.org/10.3390/d11090164
Received: 30 June 2019 / Revised: 4 September 2019 / Accepted: 9 September 2019 / Published: 13 September 2019
(This article belongs to the Special Issue Biological Invasions 2020 Horizon)

Abstract

Because biological invasions can cause many negative impacts, accurate predictions are necessary for implementing effective restrictions aimed at specific high-risk taxa. The pet trade in recent years became the most important pathway for the introduction of non-indigenous species of reptiles worldwide. Therefore, we decided to determine the most common species of lizards, snakes, and crocodiles traded as pets on the basis of market surveys in the Czech Republic, which is an export hub for ornamental animals in the European Union (EU). Subsequently, the establishment and invasion potential for the entire EU was determined for 308 species using proven risk assessment models (RAM, AS-ISK). Species with high establishment potential (determined by RAM) and at the same time with high potential to significantly harm native ecosystems (determined by AS-ISK) included the snakes Thamnophis sirtalis (Colubridae), Morelia spilota (Pythonidae) and also the lizards Tiliqua scincoides (Scincidae) and Intellagama lesueurii (Agamidae).
Keywords: Pet market; Czech Republic; introduction; pathway; ornamental animal; invasive species; snake; lizard; crocodile Pet market; Czech Republic; introduction; pathway; ornamental animal; invasive species; snake; lizard; crocodile

1. Introduction

Invasive species are considered to be among the major causes of biodiversity loss [1,2,3], and therefore conservation agencies around the world devote significant attention to this issue [4]. Time, money, and considerable effort are spent each year in the eradication, control and mitigation of non-native species [5]. However, despite the increasing interest of ecologists and conservation biologists in invasions [6], there is no sign that the introduction rate of non-indigenous species is slowing down [7].
In general, vertebrates are introduced more intentionally compared to other organisms [8]. The spread of non-native vertebrates took place in several historically specific waves and different taxonomic groups were at the peak of occupying new territories at different times. Fish, birds and mammals were introduced into new countries mainly in the 19th century and in the second half of the 20th century. On the other hand, the peak of reptile introductions was at the turn of the 20th and 21st centuries [9,10,11]—although many recent cases may have been overlooked. These differences have been caused by specificity of vectors and reasons for introductions. While fish, birds, and mammals were mostly introduced intentionally for the benefit, usually economic, of people [10], the main reason for reptile introductions is the pet trade (which makes up for about 45% of introductions), which can lead to their subsequent release or escape [12].
Increasing urbanization creates a desire for contact with nature for people living in towns and cities, and keeping pets is one way of fulfilling this need [13]. The popularity of reptiles as pets has been growing steadily since the second half of the 20th century [14,15]. Unfortunately, reptiles can have enormous negative ecological impacts, e.g., invasion of the brown tree snake (Boiga irregularis) on Guam island caused the extinction of 77% of the island’s native birds and 75% of its native lizards [16]. Also, other direct impacts on humans (e.g., (venomous) snakes or power outages caused by these snakes) cost a total of around $12 million per year [5]. One of the well-studied reptile invasions through the pet trade pathway in Europe is the case of the pond slider (Trachemys scripta). From 1989 to 1997, 52 million individual pond sliders were exported from the USA to Europe [17]. Because of the massive number of imports, they were sold very cheaply in pet shops. However, the growth of the turtle was associated with the loss of its attractive coloration and an increase in aggression, which often led unexperienced breeders to release them in the wild, where they would compete with native species of freshwater turtles for prey and places for basking [18,19]. Also, as a predator they can contribute to a local decline of native invertebrates, fish, or amphibians [20]. It is not surprising, therefore, that the import of T. s. elegans was banned by the EU’s Commission Regulation (EC) No 338/97 in 1997 (Official Journal of the European Union, 1997). Regardless of these two examples, reptiles have been widely overlooked in systematic invasion studies [21,22], and their establishment potential and invasion dynamics remain poorly understood [23].
The Czech Republic is the EU hub for the import and export of ornamental animals [24,25], and it is situated between three seas (Black, Baltic and North), which represents significant potential opportunity for the spreading of non-native species into other parts of Europe [26]. In previous articles, we evaluated invasion potential in the European Union for ornamental amphibians [27] and freshwater turtles [28] based on import data and offers from wholesalers from the Czech Republic. In this article, we complete an overview of ornamental herpetofauna by evaluating establishment potential and the impact on native ecosystems for the rest of the reptile taxonomical groups – lizards, snakes, crocodiles, and tuatara.

2. Materials and Methods

According to laws and regulations in force in the Czech Republic, the import of live animals and their products is registered by the Customs Administration of the Czech Republic. Therefore, to identify species of reptiles that are being offered in EU countries, we took species listed in materials of the Customs Administration and, additionally, surveyed the online price lists of five leading Czech wholesalers of ornamental animals and domestic producers of these animals to complete the list of potentially invasive reptiles. Furthermore, additional discussions were conducted with wholesalers and producers, who helped us clarify certain queries or provided supplementary information concerning the reptile trade, especially availability on the market. The survey was performed during the year 2016.
Altogether, 381 species from 20 families (Appendix Table A1) were identified as being on the pet market in the EU. In accordance with Nentwig et al. [29] we restricted our study to species with a native distribution entirely outside the European continent, mainly from different zoogeographical regions.
To stay consistent with previous studies about ectothermic tetrapods, we chose all states of the EU as the target region, while overseas departments and regions of France and Great Britain were not included in our study as parts of the EU [27,28].
We used two hierarchical models for determining the establishment and invasion risk: the Risk Assessment Model (RAM) for exotic amphibians and reptiles developed by the Australian Bureau of Rural Sciences [21,30] and the Aquatic Species Invasiveness Screening Kit v2.0 (AS-ISK) developed by Center for Environment Fisheries and Aquaculture Science (CEFAS) [31].
The species identified as being widely traded were firstly assessed by RAM, which tested the probability of their establishment, i.e., the formation of a self-sustaining population in a new environment [32], and then all species were evaluated for their invasion potential, i.e., their spread in the new environment simultaneously producing significant changes in the composition, structure, or processes of the ecosystem [32], in the EU by AS-ISK. We decided to use this approach mainly due to the fact that RAM is a model developed specifically for the determination of establishment only, while a major part of independently scored questions in AS-ISK deals with the potential impacts of an evaluated species rather than its ability to be introduced or established.
RAM is based on four parameters: (i) climatic similarity between the source (native distribution of species) and target regions (termed climate match risk score), (ii) species’ abilities to establish populations elsewhere (termed prop.species value), (iii) establishment success of species from the particular family (termed family random effect), and (iv) jurisdiction score, which accounts for expected variability in the establishment success rate due to the effect of a particular jurisdiction (country, state or province) and for all evaluated species is constant.
Climate match risk scores were computed using the program Climatch v1.0 (Bureau of Rural Sciences, 2008) with a Euclidean algorithm and 16 temperature and rainfall variables. This is based on comparison of data from climatic stations in the native range and data from climatic stations in the target region (EU in our case). Values of prop.species scores were computed originally for this study using the Kraus database [12]. When values for calculating prop.species or prop.genus were insufficient, we did not compute a prop.family value [22], but instead used approximation according to phylogenetically related genera i.e., the closest branches on an up-to-date phylogenetic trees. Family random effects were taken from Bomford [30]. If the value of family random effect was not listed, we substituted both potential extremes into the formula (−1.3 and 1.69), and then the range of values for risk score is presented. The risk score in RAM can reach values of 0–1, where establishment risk ranks are: low ≤ 0.16, moderate 0.17–0.39, serious 0.40–0.85 and extreme ≥ 0.86.
Not all traded species could be evaluated by the described procedure. The main problem was the impossibility of finding a map of occurrence or species living in such a small area which does not contain any climate station. Such species were therefore excluded from our analysis.
AS-ISK is an electronic toolkit which consists of 55 questions [31]. Some of the questions deal with biogeographical similarity, including the climate tolerance of the evaluated species, and some of the questions examine undesirable attributes, such as whether the species is poisonous or if it is a pathogen vector. However, most questions concern the species’ biological and ecological characteristics that can facilitate a potential invasion. There are also six questions related to climate change. For evaluating the invasion potential of ornamental reptiles, we used the sum of the scores from the questions dealing with biological and ecological features (this includes undesirable (or persistence) traits, resource exploitation, reproduction, dispersal mechanisms, and tolerance attributes). Because of the character of the questions in the AS-ISK software, we can argue that the AS-ISK invasion score from this part of the program expresses the species’ potential abilities to spread in a new environment and to alter the environment either directly or indirectly.
AS-ISK was originally developed for aquatic species. Thus, some questions (23., 44., 45. and 48.) concern characteristics related to life in a water environment. To stay consistent in our evaluation, which covers terrestrial species of reptiles, we used the term “Not applicable” as the answer for these questions across all evaluated species. The categorization (low, medium, or high invasion risk) of final numerical scores is not possible, because we did not use the AS-ISK overall score (i.e., BRA and BRA+CCA scores).
Each author of the article evaluated selected families by using both tools (RAM and AS-ISK). Before the start of the evaluation process, the authors attended three meetings for the unification of procedures and for clarifying specific issues. We searched for publications about the distribution and biology of assessed species, using their scientific names (and if necessary, their older synonyms) as search terms. Furthermore, relevant information provided on websites (www.iucn.org, https://nas.er.usgs.gov, www.animaldiversity.org), as well as literature cited therein, were used to compile published information available on selected species.

3. Results

The basics (a distribution map, or the presence of a climatic station in the area of distribution) for a climate match of the 381 evaluated species was not found or did not exist for 73 of the species (19.2%). This portion was significantly different among families (contingency tables: χ² = 42.83, P < 0.0001), with varanidae (58%), gekkonidae (68%), and agamidae (72%) being the families with the lowest number of distribution records available, or with the absence of a climatic station in their limited range of occurrence.
Only 4 species (1.30% of those with available distribution maps or climatic stations) reached the RAM extreme risk rank (Table 1). The most numerous were species with a serious RAM risk rank—111 (36.04%)—followed by 106 species with a low RAM risk rank (34.41%) and 87 species with a moderate RAM risk rank (28.25%). We took the mean value of RAM scores if species had this value noted as a range.
Values of AS-ISK were not evenly distributed (Kolmogorov-Smirnov test: D = 0.09, P < 0.05), with the greatest portion of species scores from six to nine (Figure 1). However, values of AS-ISK 13 and more were rare and reached by only fifteen species – these can be identified as having the greatest potential to harm native species in the EU (Table 2).

4. Discussion

We used a hierarchical approach to predict species’ potential establishment and spread with a negative impact on native ecosystems in the EU. In the first step, we searched for species that are imported and can be released or escape into the wild (transport and introduction). Then, using RAM, we evaluated the establishment potential of these species, and by AS-ISK, their future negative impact on EU nature. This process is advantageous because it overcomes the known problem with risk assessment models—the production of a single unifying factor such as “weediness” or “invasiveness” [33], which often leads to confusion or at least the impossibility of correcting the identification and level of expression of traits involved in the invasion process [34]. On the other hand, the procedure described has its limits. Due to the enormous number of species that were evaluated, particular families were divided among authors. While the calculation of a RAM score is not subjective and the final score is a result of mathematical procedures with given rules, the final value of the AS-ISK score for the same species can differ when species are evaluated by several authors [35,36]. We tried to adjust this by holding three meetings of the authors prior to evaluation, where unification of procedure and clarifying specific issues were discussed. It must also be mentioned that we used a non-specific jurisdiction score in the RAM formula, therefore a RAM risk score cannot be viewed as a precise estimation of the probability of establishment, but rather provides a relative ranking of ornamental reptiles traded in the EU.
In contrast to species that invade new areas through accidental pathways, transport of pet-traded species can be controlled and documented [37,38,39]. Legislative regulations can be based on negative experiences with non-native species already present in the environment, or the ban of such species can be based on predictive models of “invasivity” as a prevention [4]. This approach, which is still precise, deals firstly with the transport step of the invasion process [40]. The second step in the invasion process is introduction [41], which for pet-traded species is usually a deliberate release or unintentional escape from enclosures [12,42]. Therefore, occurrence of non-indigenous species is associated with human activity and invasions are casually linked to demographic data. It has been shown that occurrence of non-native species is associated with the density of human settlement [43], proximity of communications [32], the number of pet shops [44], wealth of inhabitants [45], or the index of urbanization [46].
Legislative regulations can effectively ban the trade of some species, however other species replace banned species to satisfy market demands – therefore we cannot expect that the volume of traded reptiles will decrease in the future [47]. Besides abiotic factors, the establishment of non-native species is influenced mostly by the number of individuals that are released into the environment, underpinned by propagule pressure [48]. For example, the potential of certain turtles to become established, which are imported as pets into the EU after the ban of Trachemys scripta, is much higher for many species than for Trachemys scripta [28]. However, their real potential to establish themselves in the EU is limited because of an increased variety of traded species [49], probably resulting in lower numbers of imported individuals for each particular species. Precise data about numbers of imported and exported individuals are still not collected by public authorities in the Czech Republic, therefore we were not able to incorporate propagule pressure into our models.
The impact of non-native species in new environments can be direct or indirect [50]. In all assessed groups of reptiles, we expect rather direct impacts – mainly competition and predation. From the evaluated species, colubrid snake Thamnophis sirtalis and Morelia spilota from the Pythonidae family exhibit high RAM scores (i.e., the ability to become established in large areas of the EU) and at the same time, high AS-ISK scores, and thus from a pan-EU perspective, they represent the most dangerous imported species.
Thamnophis sirtalis is a medium-sized snake with an extensive range from Florida in the United States to the Northwest Territories in Canada [51]. The mode of their reproduction is viviparity [52], which allows reptiles to exist even in cold climates [53]. It is very adaptable and lives in a variety of habitats, including those modified by humans such as pastureland, rural gardens, ponds, drainage canals, and ditches, and is often found near water [51]. Niche overlap is therefore assumed mainly with snakes from the Natricinae subfamily which contains three species living in the EU: Natrix natrix, Natrix maura and Natrix tessellate [54]. Competition for food would be the most probable interaction with these snakes – the food of T. sirtalis consists predominantly of anurans, salamanders, and fish [55] which are the main prey of native species of snakes from the genus Natrix [56,57,58]. A great proportion of amphibians in the EU are endangered and protected, and thus predation is another potential threat to native ecosystems. Due to its resistance to the strongest amphibian toxins, Thamnophis sirtalis can act as a nonselective predator [59]. While members of the family Colubridae are among the most successful reptile invaders in Europe with 14 % of established species among non-native reptiles in European countries [60], Thamnophis sirtalis itself was not established in Europe with known temporary occurrence in Austria, Germany, Great Britain, and Sweden [12]. While there was one case in Germany of an attempt to become established near the city of Dortmund [61], the presence in other countries was random and episodic.
Morelia spilota is a large snake reaching from two to four meters in length from the Australian zoogeographical region, where it is the most widespread python [62]. M. spilota have a broad habitat tolerance – however, occurrence of shrubs and hollow logs is critical for this semiarboreal species [62,63]. It is climatically and ecologically adaptable – in Australia it occurs in areas that receive snowfall and is also often found near human habitation [64]. Long-term persistence in adverse conditions can be facilitated by exhibition of maternal care, when females coil around their eggs and guard them until they hatch. Females leave the eggs to bask, and heat obtained from basking is transferred to the clutch. Females may also raise the temperature of the eggs by shivering [65]. The diet of adult snakes consists mainly of mammals, while juveniles consume mammals as well as reptiles [66]. In some parts of the EU, this species may become a top predator. This species may have a lifespan from 15 to 20 years [65], which also increases its invasive potential. Despite snakes from genus Morelia being popular in the pet trade [67] no record of this species outside its native range exists [12].
Other species with high values of AS-ISK evaluated in this article are large animals with the potential to become top predators in their non-native range. However, their RAM scores are low or moderate, suggesting that their potential establishment may be local and mainly in parts of south European countries. At the opposite end, the highest RAM risk scores were for small- to medium-bodied lizards. Among them, Australian medium sized lizards Tiliqua scincoides and Intellagama lesueurii also have relatively high AS-ISK scores (11 for both species). The AS-ISK score from part of the model dealing with biological and ecological features was over 10, suggesting potential strong effects on native ecosystems. Known ectothermic vertebrate pests that are already present in the EU, including the frogs Lithobates catesbeianus and Xenopus laevis, obtain this value [27].
A minority of introductions lead to establishment and spread of non-native species. For example, Europe is the continent with the most reptile introductions, but the smallest number of introductions (about 5%) lead to establishment here [12]. However, we generally underestimate the invasive potential and the negative impact of non-native species [68]. This is especially true for reptiles, which are commonly overlooked in invasion studies [21,22]. We should therefore treat each non-native reptile very carefully and in the EU, pet traded Thamnophis sirtalis, Morelia spilota, Tiliqua scincoides, and Intellagama lesueurii mainly deserve our attention.

Author Contributions

O.K. is authors of original idea. Made conceptualization, supervision and data curation. Also wrote draft of manuscript, creates methodology and visualization of results in form of tables and figures, works with literature resources. Other authors works on data analysis of assigned families in software RAM and AS-ISK and provides review of final version of manuscript draft.

Funding

This research received no external funding.

Acknowledgments

We thank Mary Bomford for her dedication to the question of risk assessment. The English was corrected by Jaroslav Janošek (correcta.cz).

Conflicts of Interest

The authors declare no conflict of interest.

Appendix

Table A1. Species of ornamental reptiles (excluding turtles) imported into EU with values of their RAM score (determining establishment potential in EU) and AS-ISK (determining potential to negatively influence nature in the EU).
Table A1. Species of ornamental reptiles (excluding turtles) imported into EU with values of their RAM score (determining establishment potential in EU) and AS-ISK (determining potential to negatively influence nature in the EU).
FamilySpeciesDistribution Map Available/Presence of Climate StationRAMAS-ISK (Biology/Ecology Score Only)
ChamaleonidaeBradypodion setaroiyes0.5084
Bradypodion thamnobatesyes0.5085
Brookesia betschyiyes0.5083
Brookesia brygooiyes0.5084
Brookesia ebenauiyes0.5080
Brookesia griveaudiyes0.5080
Brookesia minimayes0.5080
Brookesia nasusyes0.5080
Brookesia peyrierasiyes0.5080
Brookesia stumpffiyes0.5080
Brookesia therezieniyes0.5080
Brookesia thieliyes0.5081
Chamaeleo calyptratusyes0.6248
Chamaeleo dilepisyes0.7316
Chamaeleo senegalensisyes0.5443
Furcifer bifidusyes0.4503
Furcifer lateralisyes0.45010
Furcifer oustaletiyes0.45010
Furcifer pardalisyes0.4508
Furcifer verrucosusyes0.45010
Furcifer wilsiiyes0.4502
Rhampholeon acuminatusno
Rhampholeon boulengeriyes0.520−1
Rhampholeon nchisiensisno
Rhampholeon spectrumyes0.508−3
Rhampholeon spinosusyes0.508−3
Rhampholeon temporalisyes0.508−2
Rhampholeon viridisyes0.5081
Rieppelon brevicaudatusyes0.5080
Rieppeleon kersteniiyes0.5291
Trioceros bitaeniatusyes0.5867
Trioceros cristatusyes0.4506
Trioceros deremensisyes0.4503
Trioceros elliotiyes0.4619
Trioceros fuelleborniyes0.4507
Trioceros hoehneliiyes0.52811
Trioceros jacksoniiyes0.54211
Trioceros melleriyes0.4503
Trioceros montiumno
Trioceros pfefferino
Trioceros quadricornisno
Trioceros rudisyes0.4568
Trioceros werneriyes0.4506
Kinyongia boehmeiyes0.4505
Kinyongia matschieiyes0.4502
Kinyongia multituberculatayes0.4501
Kinyongia tavetanayes0.4501
Kinyongia tenuisyes0.4501
Kinyongia uthmoelleriyes0.4501
Calumma boettgeriyes0.4507
Calumma brevicorneyes0.4503
Calumma gastrotaeniayes0.4503
Calumma guillaumetino
Calumma maltheyes0.4502
Calumma marojezenseyes0.4501
Calumma nasutumyes0.4504
GekkonidaeAeluroscalabotes felinusyes0.453−2
Blaesodactylus antongilensisyes0.2410
Blaesodactylus sakalavayes0.2410
Cnemaspis africanano
Cnemaspis barbourino
Cnemaspis quattuorseriatano
Coleonyx elegansyes0.2205
Coleonyx mitratusyes0.2183
Cyrtodactylus fumosusno
Cyrtopodion scabrumyes0.5778
Elasmodactylus tetensisyes0.2411
Elasmodactylus tuberculosusyes0.2413
Eublepharis maculariusyes0.2518
Geckolepis polylepisyes0.2415
Gehyra voraxyes0.2410
Gekko badeniiyes0.1624
Gekko geckoyes0.1066
Gekko grossmanniyes0.1626
Gekko monarchusno
Gekko ulikovskiiyes0.1626
Gekko vittatusyes0.1626
Gonatodes albogularisno
Goniurosaurus lichtenfelderino
Hemidactylus ansorgiino
Hemidactylus brookiino
Hemidactylus fasciatusyes0.3699
Hemidactylus frenatusyes0.37013
Hemidactylus imbricatusyes0.38811
Hemidactylus platyurusno
Hemidactylus prashadiyes0.36910
Hemidactylus ruspoliino
Hemidactylus squamulatusno
Hemidactylus tanganicusno
Hemitheconyx caudicinctusyes0.1062
Holodactylus africanusno
Homopholis fasciatayes0.5022
Lepidodactylus lugubrisyes0.35513
Lygodactylus capensisno
Lygodactylus gutturalisno
Lygodactylus kimhowellino
Lygodactylus klemmeriyes0.1628
Lygodactylus luteopicturatusno
Lygodactylus miopsyes0.1624
Lygodactylus schefflerino
Lygodactylus williamsiyes0.1271
Matoatoa brevipesyes0.1620
Pachydactylus bibronino
Pachydactylus rangeino
Paroedura androyensisyes0.4537
Paroedura bastardiyes0.4535
Paroedura masobeyes0.4531
Paroedura pictayes0.4537
Phelsuma dubiano
Phelsuma laticaudayes0.453
Phelsuma lineatayes0.4036
Phelsuma madagascariensisyes0.4035
Phelsuma quadriocellatayes0.4033
Ptychozoon kuhlino
Ptyodactylus guttatusno
Ptyodactylus hasselquistiiyes0.06110
Ptyodactylus ragazzino
Rhacodactylus auriculatusyes0.1060
Rhacodactylus chahouayes0.1063
Rhacodactylus ciliatusyes0.1061
Sphaerodactylus sputatoryes0.2136
Stenodactylus petriiyes0.4961
Stenodactylus sthenodactylusyes0.3695
Tarentola annularisyes0.3279
Tarentola delalandiiyes0.0471
Tarentola mauretanicayes0.2741
Teratoscincus roborowskiiyes0.2131
Teratoscincus scincusyes0.2131
Tropiocolotes steudnerino
Tropiocolotes tripolitanusyes0.5051
Underwoodisaurus miliiyes0.9207
Ebenavia inunguisyes0.2413
Uroplatus ebenauiyes0.2416
Uroplatus guentheriyes0.2412
Uroplatus fimbriatusyes0.2415
Uroplatus henkeliyes0.2413
Uroplatus phantasticusyes0.2416
Chondrodactylus turnerino
Phyllopezus pollicarisyes0.2478
Stenodactylus mauritanicusyes0.5751
Diplodactylus vittatusyes0.9403
IguanidaeAnolis carolinensisyes0.30811
Basiliscus vitttatusyes0.2269
Corytophanes cristatusyes0.2717
Crotaphytus bicinctoresyes0.3265
Crotaphytus collarisyes0.3765
Ctenosaura quinquecarinatano
Ctenosaura similisyes0.4337
Dipsosaurus dorsalisyes0.5242
Gambelia wislizeniiyes0.2365
Iguana Iguanayes0.3711
Leiocephalus schreibersiyes0.3260
Phrynosoma platyrhinosyes0.3403
Sauromalus ateryes0.616−2
Sceloporus magisteryes0.2867
Sceloporus malachiticusyes0.175−1
Tropidurus hispidusno
Uta stansburianayes0.7033
Anolis coelestinusyes0.4674
Anolis cristatellusyes0.3709
Anolis cybotesyes0.4677
Anolis equestrisyes0.4398
Anolis gingivinusyes0.4677
Anolis hendersoniyes0.4677
Anolis nobleiyes0.46710
Anolis pogusyes0.4319
Anolis roquetyes0.4676
Anolis sagreiyes0.3965
Basiliscus plumifronsyes0.2262
Brachylophus fasciatusyes0.4700
Crotaphytus insularisyes0.2062
Chalarodon madagascariensisyes0.4674
Leiocephalus personatusyes0.389-2
Oplurus cyclurusyes0.4670
Oplurus fierinensisyes0.4670
Oplurus grandidieriyes0.4672
Oplurus quadrimaculatusyes0.4670
Chameleolis barbatusyes0.4674
PythonidaeAspidites ramsayiyes0.1313
Bothrochilus boayes0.0608
Broghammerus reticulatusyes0.06016
Broghammerus timoriensisyes0.0602
Leiopython albertisiiyes0.0602
Liasis macklotiyes0.0789
Morelia amethistinayes0.0789
Morelia boeleniyes0.0782
Morelia spilotayes0.76913
Morelia viridisyes0.0725
Python breitensteiniyes0.07110
Python brongersmaiyes0.0718
Python regiusyes0.0609
Python sebaeyes0.13216
BoidaeCalabaria reinhardtiiyes0.08410
Acrantophis dumeriliyes0.0849
Epicrates cenchriayes0.0608
Eunectes notaeusyes0.20614
Corallus caninusyes0.0596
Corallus hortulanusyes0.10314
Gongylophis colubrinusno
Boa constrictoryes0.17113
CrocodylidaeOsteolaemus tetraspisyes0.20115
AlligatoridaePaleosuchus palpebrosusyes0.09612
AnguidaeBarisia imbricatayes0.58–0.662
AgamidaeAcanthocercus atricollisyes0.3976
Agama aculeatayes0.4655
Agama agamayes0.20814
Agama doriaeyes0.4030
Hydrosaurus amboinensisyes0.3514
Hydrosaurus weberiyes0.3512
Japalura tricarinatayes0.4622
Leiolepis bellianayes0.1131
Leiolepis guttatayes0.1131
Leiolepis reevesiiyes0.113−2
Physignathus cocincinusyes0.2084
Intellagama lesueuriiyes0.88511
Pogona vitticepsyes0.15110
Pseudotrapelus sinaitusyes0.0877
Chlamydosaurus kingiyes0.1166
Trapelus savigniiyes0.4295
Acanthosaura lepidogasteryes0.4554
Uromastyx acanthinurayes0.0736
Uromastyx bentiyes0.058−1
Draco maculatusyes0.4553
Calotes jubatusyes0.4552
Japalura splendidano
Uromastyx geyrino
Uromastyx disparno
Uromastyx ornatano
Acanthosaura caprano
Draco volansno
Calotes emmano
Gonocephalus chamaeleontinusno
ScincidaeAcontias percivaliiyes0.2799
Bellatorias frereiyes0.1319
Egernia depressayes0.1269
Corucia zebratayes0.0641
Chalcides sexlineatusyes0.27811
Lamprolepis smaragdinayes0.2815
Mochlus sundevalliyes0.4169
Mabuya multifasciatayes0.32411
Mabuya quinquetaeniatano
Lepidothyris fernandiyes0.4119
Scincus scincusyes0.3569
Trachylepis affinisno
Trachylepis elegansyes0.2937
Trachylepis margaritiferayes0.2938
Trachylepis perrotetiino
Tiliqua gigasyes0.22610
Tiliqua scincoidesyes0.91211
Tribolonotus gracilisyes0.0649
Tropidophorus baconino
Eumeces schneideriyes0.4387
Eumeces algeriensisyes0.40510
Voeltzkowia rubrocaudatayes0.2649
GerrhosauridaeZonosaurus karsteniyes0.018–0.2718
Zonosaurus laticaudatusyes0.018–0.27110
Zonosaurus madagascariensisyes0.018–0.2716
Zonosaurus maximusyes0.018–0.2717
Zonosaurus ornatusyes0.018–0.27110
Zonosaurus quadrilineatusyes0.018–0.2716
Gerrhosaurus flavigularisno
Gerrhosaurus majoryes0.036–0.4309
Gerrhosaurus nigrolineatusno
Tracheloptychus petersiyes0.018–0.2718
VaranidaeVaranus acanthurusyes0.1199
Varanus beccariino
Varanus boehmeiyes0.1199
Varanus exanthematicusyes0.0379
Varanus jobiensisyes0.1199
Varanus macraeino
Varanus melinusno
Varanus prasinusyes0.1199
Varanus rudicolisno
Varanus salvatoryes0.11914
Varanus timorensisyes0.1198
Varanus yuwonoino
LacertidaeAcanthodactylus longipesyes0.45811
Adolfus jacksoniyes0.3913
Heliobolus spekiiyes0.4743
Holaspis guentheriyes0.3255
Latastia longicaudatayes0.49210
Takydromus sexlineatusyes0.3255
TeiidaeAmeiva ameivano
Holcosus undulatusyes0.36814
Aspidoscelis deppeiyes0.3663
Cnemidophorus lemniscatusno
Tupinambis merianaeyes0.15012
Tupinambis rufescensyes0.14512
CordylidaeCordylus beraducciiyes0.018–0.2713
Cordylus tropidosternumyes0.018–0.2713
Platysaurus guttatusno
Platysaurus intermediusyes0.019–0.2755
Platysaurus torquatusyes0.018–0.2713
ColubridaeAhaetulla nasutayes0.05610
Ahaetulla prasinayes0.0568
Coelognathus helenano
Coelognathus radiatusno
Chrysopelea ornatano
Boiga cynodonyes0.0758
Boiga dendrophilano
Coluber constrictoryes0.06712
Cyclophiops majoryes0.0608
Dasypeltis fasciatayes0.1156
Dasypeltis mediciyes0.1578
Dasypeltis scabrayes0.4018
Dromicodryas bernieriyes0.1347
Elaphe bimaculatayes0.09911
Elaphe carinatano
Erpeton tentaculatumyes0.0568
Euprepiophis mandarinusyes0.3328
Gonyosoma oxycephalayes0.3424
Homalopsis buccatayes0.1347
Lampropeltis alternayes0.0738
Lampropeltis getulayes0.12211
Lampropeltis pyromelanayes0.1168
Lampropeltis triangulumno
Lamprophis fuliginosusyes0.4829
Langaha madagascariensisyes0.1347
Leioheterodonn geayiyes0.1348
Leioheterodon madagascariensisyes0.1347
Leioheterodon modestusyes0.1347
Liophidium chabaudiyes0.1346
Madagascarophis citrinusno
Madagascarophis colubrinusyes0.1348
Nerodia taxispilotayes0.10013
Oligodon chinensisyes0.1519
Oligodon formosanusyes0.1356
Oocatochus rufodorsatusyes0.07310
Opheodrys aestivusyes0.1399
Oreocryptophis porphyraceano
Orthriophis moellendorffiyes0.2906
Orthriophis taeniurus friesino
Psammophis mossambicusyes0.1409
Psammophylax multisquamisno
Pseudelaphe flavirufayes0.0596
Rhadinophis frenatumyes0.3456
Rhamphiophis rostratusno
Rhamphiophis rubropunctatusno
Rhinocheilus leconteiyes0.1499
Rhynchophis boulengeriyes0.3426
Spalerosophis diademano
Thamnophis marcianusyes0.36913
Thamnophis sauritusyes0.35812
Thamnophis sirtalisyes0.66213
Xenochrophis vittatayes0.2907
Telescopus beetzino
Heterodon nasicusyes0.17811
Dendrelaphis cyanochlorisyes0.0567
Dendrelaphis formosusyes0.05610
Dinodon flavozonatumyes0.3446
Pantherophis vulpinusyes0.15510
Philothamnus semivariegatusyes0.7319
ViperidaeAtheris ceratophorayes0.018–0.2542
Bitis arietansyes0.101–0.67111
Bitis nasicornisyes0.019–0.2644
Bitis rhinocerosyes0.018–0.2549
Cerastes cerastesyes0.035–0.3957
Crotalus atroxyes0.057–0.5247
Crotalus cerastesyes0.026–0.3268
Cryptelytrops albolabrisno
Cryptelytrops fasciatusyes0.018–0.2544
Cryptelytrops insularisyes0.018–0.2544
Cryptelytrops purpureomaculatusyes0.018–0.2542
Trimeresurus fucatusyes0.018–0.2544
Trimeresurus nebularisyes0.018–0.2544
Trimeresurus poperiumyes0.018–0.2543
Trimeresurus puniceusyes0.018–0.2544
Tropidolaemus subannulatusyes0.018–0.2547
Tropidolaemus wagleriyes0.018–0.2543
Viridovipera gumprechtiyes0.018–0.2540
Viridovipera vogeliyes0.018–0.2540
Deinagkistrodon acutusyes0.020–0.26710
Agkistrodon contortrixyes0.082–0.6208
ElapidaeAcanthopis praelongusyes0.126−1
Aspidelaps lubricusyes0.4051
Dendroaspis angusticepsyes0.4183
Naja atrayes0.2163
Naja kaouthiayes0.3815
Naja najayes0.1709
XenopeltidaeXenopeltis unicoloryes0.1907
SphenodontidaeSphenodon punctatusyes0.072–0.6074

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Figure 1. Distribution of AS-ISK score (from Biology/Ecology section only) of ornamental reptile species (excluding turtles) for the EU area.
Figure 1. Distribution of AS-ISK score (from Biology/Ecology section only) of ornamental reptile species (excluding turtles) for the EU area.
Diversity 11 00164 g001
Table 1. Species of ornamental reptiles (excluding turtles) with highest potential to establish viable populations in the EU, based on the Risk Assessment model.
Table 1. Species of ornamental reptiles (excluding turtles) with highest potential to establish viable populations in the EU, based on the Risk Assessment model.
SpeciesFamilyRisk ScoreRisk Rank
Diplodactylus vittatusGekkonidae0.940extreme
Underwoodisaurus miliiGekkonidae0.920extreme
Tiliqua scincoidesScincidae0.912extreme
Intellagama lesueuriiAgamidae0.885extreme
Morelia spilotaPythonidae0.769serious
Philothamnus semivariegatusColubridae0.731serious
Chamaeleo dilepisChamaeleonidae0.730serious
Uta stansburianaIguanidae0.703serious
Thamnophis sirtalisColubridae0.662serious
Chamaeleo calyptratusChamaeleonidae0.624serious
Barisia imbricataAnguidae0.582–0.663serious
Sauromalus aterIguanidae0.616serious
Trioceros bitaeniatusChamaeleonidae0.586serious
Cyrtopodion scabrumGekkonidae0.577serious
Stenodactylus mauritanicusGekkonidae0.575serious
Table 2. Species of ornamental reptiles (excluding turtles) with highest potential to spread and negatively influence nature in the EU, based on AS-ISK (from the Biology/Ecology section only).
Table 2. Species of ornamental reptiles (excluding turtles) with highest potential to spread and negatively influence nature in the EU, based on AS-ISK (from the Biology/Ecology section only).
SpeciesFamilyRisk Score
Python sebaePythonidae16
Malayopython reticulatusPythonidae16
Osteolaemus tetraspisCrocodylidae15
Agama agamaAgamidae14
Eunectes notaeusBoidae14
Varanus salvatorVaranidae14
Corallus hortulanusBoidae14
Holcosus undulatusTeiidae14
Hemidactylus frenatusGekkonidae13
Lepidodactylus lugubrisGekkonidae13
Morelia spilotaPythonidae13
Boa constrictorBoidae13
Nerodia taxispilotaColubridae13
Thamnophis marcianusColubridae13
Thamnophis sirtalisColubridae13
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