Research Article |
Corresponding author: Andrey N. Reshetnikov ( anreshetnikov@yandex.ru ) Academic editor: Katelyn Faulkner
© 2023 Andrey N. Reshetnikov, Marina G. Zibrova, Dinçer Ayaz, Santosh Bhattarai, Oleg V. Borodin, Amaël Borzée, Jindřich Brejcha, Kerim Çiçek, Maria Dimaki, Igor V. Doronin, Sergey M. Drobenkov, Uzlipat A. Gichikhanova, Anastasia Y. Gladkova, Dmitriy A. Gordeev, Yiannis Ioannidis, Mikhail P. Ilyukh, Elena A. Interesova, Trupti D. Jadhav, Dmitry P. Karabanov, Viner F. Khabibullin, Tolibjon K. Khabilov, M. Monirul H. Khan, Artem A. Kidov, Alexandr S. Klimov, Denis N. Kochetkov, Vladimir G. Kolbintsev, Sergius L. Kuzmin, Konstantin Y. Lotiev, Nora E. Louppova, Vladimir D. Lvov, Sergey M. Lyapkov, Igor M. Martynenko, Irina V. Maslova, Rafaqat Masroor, Liudmila F. Mazanaeva, Dmitriy A. Milko, Konstantin D. Milto, Omid Mozaffari, Truong Q. Nguyen, Ruslan V. Novitsky, Andrey B. Petrovskiy, Vladimir A. Prelovskiy, Valentin V. Serbin, Hai-tao Shi, Nikolay V. Skalon, Richard P. J. H. Struijk, Mari Taniguchi, David Tarkhnishvili, Vladimir F. Tsurkan, Oleg Y. Tyutenkov, Mikhail V. Ushakov, Dmitriy A. Vekhov, Fanrong Xiao, Andrey V. Yakimov, Tatyana I. Yakovleva, Peimin Yang, Dmitriy F. Zeleev, Varos G. Petrosyan.
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Citation:
Reshetnikov AN, Zibrova MG, Ayaz D, Bhattarai S, Borodin OV, Borzée A, Brejcha J, Çiçek K, Dimaki M, Doronin IV, Drobenkov SM, Gichikhanova UA, Gladkova AY, Gordeev DA, Ioannidis Y, Ilyukh MP, Interesova EA, Jadhav TD, Karabanov DP, Khabibullin VF, Khabilov TK, Khan MMH, Kidov AA, Klimov AS, Kochetkov DN, Kolbintsev VG, Kuzmin SL, Lotiev KY, Louppova NE, Lvov VD, Lyapkov SM, Martynenko IM, Maslova IV, Masroor R, Mazanaeva LF, Milko DA, Milto KD, Mozaffari O, Nguyen TQ, Novitsky RV, Petrovskiy AB, Prelovskiy VA, Serbin VV, Shi H-t, Skalon NV, Struijk RPJH, Taniguchi M, Tarkhnishvili D, Tsurkan VF, Tyutenkov OY, Ushakov MV, Vekhov DA, Xiao F, Yakimov AV, Yakovleva TI, Yang P, Zeleev DF, Petrosyan VG (2023) Rarely naturalized, but widespread and even invasive: the paradox of a popular pet terrapin expansion in Eurasia. NeoBiota 81: 91-127. https://doi.org/10.3897/neobiota.81.90473
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The North American terrapin, the red-eared slider, has globally recognized invasive status. We built a new extensive database using our own original and literature data on the ecology of this reptile, representing information on 1477 water bodies throughout Eurasia over the last 50 years. The analysis reveals regions of earliest introductions and long-term spatio-temporal dynamics of the expansion covering now 68 Eurasian countries, including eight countries reported here for the first time. We established also long-term trends in terms of numbers of terrapins per aquatic site, habitat occupation, and reproduction success. Our investigation has revealed differences in the ecology of the red-eared slider in different parts of Eurasia. The most prominent expression of diverse signs of invasion success (higher portion of inhabited natural water bodies, higher number of individuals per water body, successful overwintering, occurrence of juvenile individuals, successful reproduction, and establishment of populations) are typical for Europe, West Asia and East Asia and tend to be restricted to coastal regions and islands. Reproduction records coincide well with the predicted potential range based on climatic requirements but records of successful wintering have a wider distribution. This invader provides an excellent and possibly unique (among animals) example of wide alien distribution, without the establishment of reproducing populations, but through the recruitment of new individuals to rising pseudopopulations due to additional releases. Therefore, alongside the potential reproduction range, a cost-effective strategy for population control must take in account the geographical area of successful wintering.
Alien species, biological invasions, global change, invasion ecology, nature conservation, wintering
The growth of the global human population and the development of international transport networks has resulted in mass translocations of biological species outside of their native ranges, that have led to the homogenization of the Earth’s biota within potential ecological niches (
The invasion of alien amphibians and reptiles has significantly accelerated since the middle of 20th century (
Young red-eared slider individuals are small and brightly colored, making them very attractive for aquarists. However, these animals grow rapidly, and large individuals require more space, are less visually appealing, aggressive and may bite. Releasing them into the nearest water body is a common way to get rid of an annoying pet. This terrapin easily adapts to outdoor conditions and can reproduce and establish stable populations in regions with an appropriate climate (
Despite biosecurity efforts in some countries, today the pond slider (mainly red-eared slider) occurs in outdoor water bodies on all continents except Antarctica (
Modelling of potential ranges of species is a popular direction of contemporary ecology; analyses have been performed for the red-eared slider, mainly at the species level using available datasets and on different geographic scales (e.g.,
Different definitions of the term “invasive species” have been proposed based on ecological and/or practical approaches (e.g.,
For assessing the current distribution, the verified original records of the red-eared slider from 236 geographic localities were collected by the authors of this paper during their field inspections of water bodies in different regions of Eurasia in 2002–2020. Additionally, 1241 relevant records from 1968–2020 were obtained from scientific papers (Suppl. material
The geographical distribution of the red-eared slider Trachemys scripta elegans in Eurasia. a sources of data: 1 (red squares) – records from literature sources (see Suppl. material
We used earlier suggested terms (
We used all available georeferenced data (1968–2020) to understand the invasion ecology of this reptile in regions of Eurasia. Some original and literature records indicated habitat characteristics (N=1219), number of sliders per water body (N=963), measure of slider sizes (carapace length, CL, with accuracy ± 1cm) and/or distant assessing of sizes (with an interval of 5cm) (N=570), and information on ecology (N=270). The proportion of records with appropriate data are presented for each part of Eurasia separately in Table
Proportion of records (%) with appropriate data for each part of Eurasia.
Europe | E Asia | N Asia | W Asia | S Asia | SE Asia | C Asia | |
---|---|---|---|---|---|---|---|
Habitats | 82.3 | 89.8 | 100 | 83.6 | 24.0 | 38.5 | 100 |
Numbers | 75.3 | 54.5 | 95.2 | 93.4 | 22.0 | 33.3 | 100 |
Sizes | 33.1 | 40.7 | 85.7 | 78.7 | 26.0 | 35.9 | 25 |
Ecology | 26.2 | 6.1 | 4.8 | 50.8 | 6.0 | 28.2 | 100 |
We used data on latitude, longitude, date, habitat characteristics, number of individuals per water body, body sizes, and ecology to build correlation matrixes. Some parameters (habitat characteristics, body sizes, and ecology) were ranked as presented in Suppl. material
We aimed to build two species distribution models (SDM) for red-eared slider: (a) the potential range of successful reproduction as an assessment of the probable area of population establishment (SDM1); (b) the potential range of successful overwintering as a probable area of long-term survival of released individuals (SDM2). The models were built using four sequential steps: (i) preparation of vector and raster layers; (ii) thinning of environmental variables and georeferenced records; (iii) selection of background areas for MaxEnt models; (iv) determination of MaxEnt model parameters; (v) building SDMs using MaxEnt.
In our case, the maximum Pearson coefficient was PC=0.742 between the variables BIO10 and growingdegdays0, and the maximum VIF=6.8 for the variable BIO10.
We used a two-step procedure to identify and reduce the spatial autocorrelation of georeferenced records. We used the spThin package in R (
To analyze the features of environmental factors favorable for successful reproduction of the studied terrapin, a comparative analysis of the centroids (mean positions of species localities in relation to environmental factors) of niches for several predictor variables in three parts of the range (Europe, West Asia, and East Asia) was carried out. These parts of the range were selected because of sufficient records of four ecological characteristics: confirmed successful overwintering, unsuccessful reproduction attempts, confirmed successful reproduction, and established populations. Comparative analysis was performed using GLM ANOVA (see section Statistics) based on raw values of ecologically important predictor variables (BIO10, BIO18, growingDegDays0, climaticMoistureIndex the same as used for the SDMs – see the methodology above).
Normalized histograms were used for visualization of data on invasion ecology; means and standard errors are shown in the text as descriptive statistics. Spearman R rank correlation coefficient was applied for assessing possible relationships between measures of invasion ecology, date, and latitude and longitude. Statistical hypotheses were tested at 0.05 p-level. Multiple comparisons of the proportion of key habitat use by the red-eared slider in the three parts of the invaded range (Europe, West Asia, East Asia) for which there were enough data for appropriate statistical analysis was performed using the chi-square statistical test and then the Tukey Post hoc test (
Comparative analysis of niche centroids was made using the Generalized Linear Model (GLM) procedure. In this model, one way analysis of variance (ANOVA) was used with equal and unequal numbers of replicates in the cells. In all cases, type I analysis of variance models was used, i.e., fixed factor models. In the first ANOVA model we used the factor “geographic region” and compared species niche centroids (means of predictor variables) in different geographic regions (Europe, West Asia, and East Asia), i.e. we used one-way ANOVA with three levels of region factors. For the second group of the models, the factor “establishment success” was used, consisting of four levels of reproductive/establishment status (see above). This analysis is important to identify the range of environmental parameters favorable for successful reproduction. If an analysis of variance with fixed effects showed a significant difference in the level of factors, a test of multiple comparison, the Post hoc Tukey HSD was used to determine which levels of the factor differed from each other. For multiple comparisons with unequal variances according to Leuven’s test, the Tukey-Cramer test with Welch’s modification was used (
Statistical analysis was performed using basic and special packages in the R language in RStudio Version 1.2.5033 (
Records from 1968–1989 fall into countries in Europe, West Asia, and East Asia. The earliest records were reported from the Czech Republic from 1968, southern Japanese islands from 1972, Israel from 1975, the Netherlands from 1980, and Belgium from 1982. Records from 1990–1999 occurred in more regions of Europe, West Asia, East Asia and expanded to Southeast Asia (the Czech Republic, Spain, Italy, Sweden, England, Romania, Germany, Belgium, the Netherlands, Poland, Israel, Japan, Thailand, Vietnam, Republic of Korea and the Taiwan Island). By 2010 this reptile was already known in all parts of Eurasia, except Central Asia and North Asia, but today it occurs in all parts of Eurasia. Spatio-temporal dynamics of records are shown in Fig.
In the most studied parts of the continent, i.e., Europe and East Asia, the proportion of records in parks and other urban environments reaches 83.8 and 82.6% respectively (Fig.
Ecological characteristics (left axis, %) and numbers of observations (at the tops of columns) of the red-eared slider Trachemys scripta elegans in different parts of Eurasia. a habitats: sites outside human settlements (“nature”); urban sites outside recreational zones (“urban sites”); public parks b number of individuals per water body (n) c body sizes (cm) d ecology: wintering; unsuccessful reproductive attempts; successful reproduction; establishment of populations. Colors are explained in the legends.
Distribution of red-eared sliders among the three types of habitats does not differ between the European and East Asian parts of the range, but habitat distribution in both regions significantly differe from habitat distribution in West Asia (Fig.
Comparison of the distribution of red-eared sliders among habitats in three different parts of the Eurasian invaded range. See details of habitat coding in Suppl. material
The three regions with the highest number of observations, Europe, West Asia, and East Asia (Fig.
Diversity and proportions of observations (not water bodies) of various size classes of red-eared slider in parts of Eurasia are presented at Fig.
Analysis of indices of the size diversity of terrapin individuals showed that in East Asia, Shannon’s index (H = 1.53 ± 0.012) is higher than in Europe (H = 1.38 ± 0.015) and West Asia (H = 0.19 ± 0.032), i.e., body size diversity in East Asia is higher than in the other two parts of the range (Fig.
In all parts of Eurasia, except West Asia, the highest number of observations are casual records of red-eared sliders without additional information on ecology. For example, in the most studied regions, Europe and East Asia, the appropriate percentages of casual records are 73.8 and 93.9%, respectively. Multiple cases of unsuccessful reproduction attempts (e.g., egg laying) were registered in Europe and the Trans-Caucasus region, whereas successful reproduction and even establishment of populations is reported from southern Europe, West Asia, East Asia, and Southeast Asia (Figs
In Europe, reproduction is more effective in southwestern regions and positively correlates with terrapin abundance (see Suppl. material
Potential distribution of the red-eared slider Trachemys scripta elegans, created with MaxEnt analysis of climatic requirements. a potential range of successful reproduction. Species Distribution Model has been built based on records of the native range of the red-eared slider within Northern America and records of successful reproduction and established populations within Eurasia (which are shown by yellow points) b potential range of successful wintering. Species Distribution Model has been built based on records used for Fig.
Comparison of the mean values of the predictor variables shows that the niche centroids of the species in East Asia are characterized by relatively high values of mean air temperature in the warm season (T = 26.01 ± 0.46 °C, n = 35), precipitation (W = 676.4 ± 15.4, mm), climate moisture index (Mi = 0.4 ± 0.03), and total temperature above 0 °C (SigmaT = 7.78 * 104 ± 3207 °C) (Fig.
Comparison of mean values (± 95% Tukey HSD confidence intervals) of the main predictor variables of terrapin habitats in different parts of the invaded range. The results of one factor ANOVA based on General Linear Model are presented. The GLM ANOVA tested the main effects of regions: a F = 78.31, df = 2, p < 0.01 b F = 424.21, df = 2, P< 0.01 c F = 196.42, df = 2, p < 0.01 d F = 58.62, df = 2, p < 0.01 (F is Tukey HSD test; P-value is given for the factor effects). Significant differences of means according to Post hoc Tukey HSD test are marked by *. Absence of significant differences is marked as NS, i.e., values for Europe and West Asia do not differ from each other on Fig.
A comparative analysis of the parameters of reproductive efforts in Eurasia showed that centroids 2 and 3 (wintering and egg laying) significantly differ from 4 and 5 (successful reproduction and establishment of populations) (Fig.
Comparison of mean values (± 95% Tukey HSD confidence intervals) of main predictor variables of terrapin habitats for records with different ecological/reproductive statuses. The results of one factor ANOVA based on General Linear Model (GLM) are presented. The GLM ANOVA tested the main effects of reproduction status (where 2 is confirmed successful overwintering; 3 is unsuccessful reproduction attempts, 4 is confirmed successful reproduction, 5 is established population): a F=23.5, df = 3, p < 0.01 b F = 20.92, df = 3, p < 0.01 c F = 19.7, df = 3, p < 0.01 d F = 24.4, df = 3, p < 0.01 (F is Tukey HSD test; p value is given for the factor effects). Statistically significant differences of means according to Post hoc Tukey HSD test between 4 and 2, 3 (separately) is marked by *; statistically significant differences of means between 5 and 2, 3 (separately) is marked by **. We did not compare means of categories 2 and 3 as they are rather similar. The same is true for 4 and 5.
The earliest reports of the red-eared slider in outdoor water bodies of Eurasia originate from the late 1960s – early 1970s in Europe (Rumburk, Czech Republic), where this animal was recorded in 1968 (
Of course, data on ecological characteristics of the red-eared slider for some water bodies may be absent due to lack of appropriate observations. Nevertheless, our large-scale spatio-temporal approach (invasion within all of Eurasia during a 50-year period) reduces possible inaccuracies and allows us to reconstruct the invasion process within the studied continent. Our comprehensive database of primary data allowed us to compare ecological features of the red-eared slider in different parts of Eurasia. We found that the ecological niche of reproductive groups of the red-eared slider in East Asia differs from those in Europe and West Asia in terms of thermal energy and moisture (Fig.
Importantly, the red-eared slider inhabits mainly urban and rural environments (Fig.
Recorded red-eared slider numbers may entirely (in regions without reproduction) or partly (in regions with reproduction) reflect past human activities, i.e., accumulation of human-released slider individuals, a phenomenon defined as “invasion debt” (
Our results show a higher density of records of the slider in Europe and East Asia (Fig.
Reproductive success depends on several key environmental parameters (Fig.
In the current analysis (Fig.
The results of all the species distribution models have some differences due to variations in datasets and climatic variable sets used. The calculated reproductive range of the red-eared slider in Eurasia in our study (Fig.
The invasive status of a species assumes 1) naturalization, i.e., establishment of populations, and 2) remarkable negative impact on native species/ecosystems (
Successful wintering is registered for all parts of the continent (Figs
We propose the “range of successful wintering” as a territory at risk for true invasion as well as for conditional invasion. This non-standard (for a reptile) characteristic, i.e., wintering range, must be taken in account when planning eradication campaigns or other measures of control of the red-eared slider.
The geographical expansion of the red-eared slider started in the 1960–1970s from two opposite sides of Eurasia, i.e., Europe and East Asia, and was driven by massive propagule pressure in different regions over its huge territory. The invasive range of this terrapin enlarged gradually in Eurasia up to the beginning of the 2020s covering 68 Eurasian countries. In particular, we report original data outlining recent first detections of this alien terrapin in the following countries: Bangladesh, Georgia, Kazakhstan, Kyrgyzstan, Mongolia, Nepal, Pakistan, Tajikistan, as well as Russian Siberia (drainages of rivers Ob and Yenisei). Regions of successful reproduction of this ectotherm in Eurasia are well-predictable on the basis of climatic features of the native geographic range but may be altered because of progressing global climate change. Analyses of invasion ecology confirm that coastal regions and islands show the most prominent expression of diverse signs of invasion success in terms of a higher portion of inhabited natural water bodies, higher number of individuals per water body, successful overwintering, occurrence of juvenile individuals, successful reproduction, and establishment of populations. Notably, a great number of established groups of this reptile in different regions of Eurasia do not meet the conditions for successful reproduction.
In this pet terrapin we have an excellent but rare example of wide geographic expansion without the establishment of (reproducing) populations but through the recruitment of new individuals to growing (non-reproducing) pseudopopulations due to additional releases. Therefore, we highlight the significance of the wintering range. This range must be taken in account when planning measures of control of this invader because non-reproducing groups of this terrapin may become a significant component of freshwater ecosystems with impact on native species. Thus, a cost-effective conservation strategy against the red-eared slider in large countries with a variety of climatic zones may differ for three geographical areas: 1) area of true invasion (within potential reproduction range), 2) area of conditional invasion (within potential wintering range but outside potential reproduction range), and 3) area without potential for reproduction and wintering. Nevertheless, some protective measures (i.e., banning of import and trade) are effective only on an all-country level and therefore must be applied at national levels. Finally, we encourage further accumulation of empirical knowledge on the invasion ecology of the red-eared slider in newly-invaded regions, especially in North Asia and South Asia, to establish a deeper understanding of its adaptive limits and role in Eurasian native ecosystems.
We are thankful to subject editor K. Faulkner and two anonymous reviewers for valuable suggestions on the manuscript, M. Vamberger for discussion of terrapin ecology in Germany, J. Lovich for discussion of subspecies features, N.N. Suryadna for discussion of records in the Black Sea region, T.V. Abduraupov, Pritpal Soorae and D. Verbelen for help with literature in Uzbekistan, UAE and Belgium respectively, T. Rautenberg for providing photographs for identification of terrapins observed in Essen. We greatly appreciate A.V. Zhulina and A.A. Zibrova for their help with an illustration for a Suppl. material, photographer E.S. Malafeeva for portrait of red-eared slider for graphical abstract, and J.A. Titova for linguistic corrections. We are also sincerely grateful to the 52 persons who kindly provided the additional observations of red-eared sliders in open water bodies of Eurasia (the full list of the persons see in the Suppl. material
List of literature sources with records of red-eared slider in Eurasia
Data type: Pdf file
Eurasian subregions as accepted in the current article
Data type: Pdf file
Data base of georeferenced records of Trachemys scripta elegans in Eurasia
Data type: xls file
Coding of collected field data
Data type: Pdf file
Correlation matrix for ecological and other parameters of the red-eared slider Trachemys scripta elegans in water bodies of Europe (a), West Asia (b) and East Asia (c)
Data type: Pdf file
Locations of the training areas based on the available occurrence records
Data type: Pdf file
Evaluation metrics for MaxEnt models made across a range of feature-class combinations and regularization multipliers
Data type: Pdf file
Comparison of mean values of the Log-transformed predictor variables
Data type: Pdf file
Original list of 68 Eurasian countries colonized by the red-eared slider Trachemys scripta elegans
Data type: Pdf file
Additional list of 52 persons who kindly provided their observations of red-eared sliders in open water bodies of Eurasia
Data type: Pdf file