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Rarely naturalized, but widespread
and even invasive: the paradox of
a popular pet terrapin expansion in Eurasia
Andrey N. Reshetnikov1, Marina G. Zibrova1, Dinçer Ayaz2,
Santosh Bhattarai3, Oleg V. Borodin4, Amaël Borzée5, Jindřich Brejcha6,
Kerim Çiçek2, Maria Dimaki7, Igor V. Doronin8, Sergey M. Drobenkov9,
Uzlipat A. Gichikhanova10, Anastasia Y. Gladkova11, Dmitriy A. Gordeev12,
Yiannis Ioannidis13, Mikhail P. Ilyukh14, Elena A. Interesova15,
Trupti D. Jadhav16, Dmitry P. Karabanov17, Viner F. Khabibullin18,
Tolibjon K. Khabilov19, M. Monirul H. Khan20, Artem A. Kidov1,
Alexandr S. Klimov21, Denis N. Kochetkov22, Vladimir G. Kolbintsev23,
Sergius L. Kuzmin1, Konstantin Y. Lotiev24, Nora E. Louppova1,
Vladimir D. Lvov25, Sergey M. Lyapkov1, Igor M. Martynenko26,
Irina V. Maslova27, Rafaqat Masroor28, Liudmila F. Mazanaeva10,
Dmitriy A. Milko29, Konstantin D. Milto8, Omid Mozaari30,
Truong Q. Nguyen31, Ruslan V. Novitsky9, Andrey B. Petrovskiy1,
Vladimir A. Prelovskiy32, Valentin V. Serbin33, Hai-tao Shi34,
Nikolay V. Skalon35, Richard P. J. H. Struijk36, Mari Taniguchi37,
David Tarkhnishvili38, Vladimir F. Tsurkan39, Oleg Y. Tyutenkov15,
Mikhail V. Ushakov21, Dmitriy A. Vekhov26, Fanrong Xiao34,
Andrey V. Yakimov25, Tatyana I. Yakovleva18, Peimin Yang40,
Dmitriy F. Zeleev4, Varos G. Petrosyan1
1Unaliated, Moscow, Russia 2Zoology Section, Department of Biology, Faculty of Science, Ege University,
Bornova, Izmir, Turkiye 3 Nepal Conservation and Research Center, Nepal 4 Unaliated, Ulyanovsk,
Russia 5 Laboratory of Animal Behaviour and Conservation, College of Biology and the Environment,
Nanjing Forestry University, Nanjing, People’s Republic of China 6Department of Philosophy and History
of Science, Faculty of Science, Charles University in Prague, Praha, Czech Republic 7Goulandris Natural
History Museum, Kissia, Greece 8Unaliated, St. Petersburg, Russia 9 Science-Practical Center of the
National Academy of Sciences of the Republic of Belarus for Bioresources, Minsk, Belarus 10Unaliated,
Makhachkala, Russia 11Unaliated, Borisovka, Russia 12Unaliated, Volgograd, Russia 13Ecostudies PC,
Athens, Greece 14Unaliated, Stavropol, Russia 15Unaliated, Tomsk, Russia 16Department of Zoology,
Dhempe College of Arts and Science, Miramar, India 17Unaliated, Borok, Russia 18Unaliated, Ufa,
Russia 19Institute of Natural Sciences of Khujand State University, Khujand, Tajikistan 20Jahangirnagar
University, Dhaka, Bangladesh 21Unaliated, Voronezh, Russia 22Unaliated, Arkhara, Russia 23Aksu-
NeoBiota 81: 91–127 (2023)
doi: 10.3897/neobiota.81.90473
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RESEARCH ARTICLE
Advancing research on alien species and biological invasions
A peer-reviewed open-access journal
NeoBiota
Andrey N. Reshetnikov et al. / NeoBiota 81: 91–127 (2023)
92
Zhabagly Nature Reserve, Zhabagly, Kazakhstan 24Unaliated, Sochi, Russia 25Unaliated, Nalchik,
Russia 26 Unaliated, Rostov-on-Don, Russia 27Unaliated, Vladivostok, Russia 28 Zoological Sciences
Division, Pakistan Museum of Natural History, Islamabad, Pakistan 29 Institute of Biology National
Academy of Sciences, Bishkek, Kyrgyz Republic 30Aria Herpetological Institute, Tehran, Iran 31Institute
of Ecology and Biological Resources, Graduate University of Science and Technology, Vietnam Academy of
Science and Technology, Hanoi, Vietnam 32 Unaliated, Irkutsk, Russia 33Unaliated, Taman, Russia
34Key Laboratory for Ecology of Tropical Islands of Ministry of Education, Key Laboratory of Tropical Animal
and Plant Ecology of Hainan Province, College of Life Sciences, Hainan Normal University, Hainan, China
35Unaliated, Kemerovo, Russia 36Reptile, Amphibian and Fish Conservation Netherlands (RAVON),
Nijmegen, e Netherlands 37Nature Recovery Co., Ltd., Kobe, Japan 38School of Natural Sciences and
Medicine, Ilia State University, Tbilisi, Georgia 39 Institut of Zoology, Chişinău, Republic of Moldova
40Liaoning Key Laboratory for Prevention and Treatment of Aquatic Animal Diseases, Freshwater Fisheries
Research Academy of Liaoning Province, Liaoyang, China
Corresponding author: Andrey N. Reshetnikov (anreshetnikov@yandex.ru)
Academic editor: Katelyn Faulkner|Received 16 July 2022|Accepted 3 January 2023|Published 24 January 2023
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, Mozaari 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
Abstract
e 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. e 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 rst 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 dierences in the ecology of the red-eared slider in dierent parts of Eurasia. e
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. is 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. erefore,
alongside the potential reproduction range, a cost-eective strategy for population control must take in
account the geographical area of successful wintering.
e paradox of a popular pet terrapin expansion in Eurasia 93
Graphical abstract
Keywords
Alien species, biological invasions, global change, invasion ecology, nature conservation, wintering
Introduction
e 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 po-
tential ecological niches (McKinney and Lockwood 1999; Seebens et al. 2020). Inten-
tional and unintentional biological invasions represent considerable issues for native
biodiversity, economic activities and even human health (Gilpin 1990; Vitousek et al.
1996; Mazza et al. 2014).
e invasion of alien amphibians and reptiles has signicantly accelerated since
the middle of 20th century (Kraus 2009; Capinha et al. 2017). Alongside the brahminy
blindsnake Indotyphlops braminus and common house gecko Hemidactylus frenatus, the
Andrey N. Reshetnikov et al. / NeoBiota 81: 91–127 (2023)
94
pond slider Trachemys scripta (Schoep, 1792) is one of the three most widespread alien
reptiles globally (Capinha et al. 2017). e native range of the pond slider Trachemys
scripta is restricted to central, southern and southeastern United States and the adjacent
portion of Mexico (Rhodin et al. 2017). is species of terrapin consists of at least three
subspecies. Subspecies T. s. scripta (yellow-bellied slider) and T. s. troostii (Cumberland
slider) are kept and bred in captivity substantially less often compared with T. s. elegans
(red-eared slider). e last taxon became very popular as a pet animal, sometimes also
an ornamental pond animal, and has been one of the most-traded reptiles since the
middle of the 20th century. Export from the United States to other countries reached
millions of individuals per year (Telecky 2001; Reed and Gibbons 2003). Since the
end of 20th century, large-scale commercial breeding of T. s. elegans also started in
China and countries of Southeast Asia where it is used for human consumption (van
Dijk et al. 2000). ese active and mobile reptiles often escape captivity.
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.
is terrapin easily adapts to outdoor conditions and can reproduce and establish
stable populations in regions with an appropriate climate (Rödder et al. 2009; Heidy
Kikillus et al. 2010). Once established, the slider may induce a negative impact on
native macrophytes and hydrobionts (Ficetola et al. 2012). Amphibians are regarded
to be especially vulnerable because this terrapin feeds on tadpoles, and the presence
of chemical cues released by this predator can aect the development rate and size at
metamorphosis of tadpoles (Polo-Cavia et al. 2010; Vodrážková et al. 2020). e red-
eared slider is more aggressive and has higher reproductive characteristics and, hence,
may successfully compete with native terrapin species for food, basking sites and,
possibly, egg-laying places (Cadi and Joly 2003; Perez-Santigosa et al. 2008; Pérez-
Santigosa et al. 2011; Polo-Cavia et al. 2011; Pearson et al. 2015). Experimental
studies have conrmed a higher mortality of native European pond terrapin in the
presence of the invasive red-eared slider (Cadi and Joly 2004). In addition, this alien
terrapin can induce the genetic pollution of populations of native terrapins due to
introgression (Parham et al. 2013) and is involved in the life cycles of native parasite
species, while also acting as a vector for the invasion of alien parasites, which are
capable of infecting native terrapins and increase the risk of epizootics, causing mass
mortalities (Iglesias et al. 2015; Demkowska-Kutrzepa et al. 2018). Moreover, this
alien reptile can carry the agents of salmonellosis, which is dangerous for human
health (Nagano et al. 2006; Shen et al. 2011). For these reasons, the trade of small-
sized (<10 cm) individuals of red-eared slider was banned in the 1970s in the United
States and import of this reptile to Europe has been entirely banned since 1997
(Ficetola et al. 2012).
Despite biosecurity eorts in some countries, today the pond slider (mainly
red-eared slider) occurs in outdoor water bodies on all continents except Antarctica
e paradox of a popular pet terrapin expansion in Eurasia 95
(Ramsay et al. 2007; Ficetola et al. 2012; Rhodin et al. 2017). e invasive ranges
of the pond slider T. scripta and its subspecies T. s. elegans in some regions of Eurasia
were recently reected in several scientic reviews (Sillero et al. 2014; Rhodin et al.
2017). However, regions of Eurasia signicantly dier in volumes of primary data.
e best studied region is West Europe (Sillero et al. 2014) whereas huge areas of
North Asia, South Asia, and Middle and Central Asia (marked below as Central Asia)
are commonly depicted as a blank spot, reecting the absence of appropriate studies
(Rödder et al. 2009; Heidy Kikillus et al. 2010; Ma and Shi 2017; Rhodin et al. 2017).
Detecting the alien terrapins is easy in park ponds during warm seasons but may be
a dicult task when direct spotting is limited by seasonality, weather (especially in
northern regions), large water body size, macrophyte densities, and landscape features.
In those cases, indirect express methods of detection, such as detection dogs, e-DNA or
parasitological analysis of co-inhabiting hydrobionts, may be applied (O’Keee 2009;
Kakuda et al. 2019; Reshetnikov and Sokolov 2020).
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 dierent geographic scales (e.g., Ficetola et al.
2009; Rödder et al. 2009; Heidy Kikillus et al. 2010; Masin et al. 2014; Banha et al.
2017). However, physiological dierences of subspecies are debatable and individuals
of other subspecies are less common in regions outside their native distribution. Im-
portantly, additional primary data from extensive, previously unstudied, regions can
alter knowledge about its niche and, hence, its potential distribution.
Dierent denitions of the term “invasive species” have been proposed based on
ecological and/or practical approaches (e.g., Jeschke and Strayer 2005; Beck et al.
2008; Blackburn et al. 2011). We suggest that the main features of an invasive alien
taxon are establishment of self-sustaining populations and their signicant eect on
native ecosystems. Due to assumed negative inuences on freshwater ecosystems,
the widely spread subspecies T. s. elegans, is regarded as an invasive taxon in Europe
and North Asia (European Commission 2016; Reshetnikov et al. 2018). However,
despite the large volume of scientic publications on this animal, to date, data on
negative impact of the red-eared slider upon native species are scarce in most regions
of Eurasia (but see: Cadi et al. 2004; Perez-Santigosa et al. 2008) and geographic
limits of its invasive populations are still debatable because conrmation of its
successful reproduction is a complex task (Cadi and Joly 2004). We hypothesized
that the invasion ecology, including establishment of populations, of this reptile in
dierent colonized areas may dier and thus the invasive status of red-eared slider
needs to be reviewed. A distinguishing feature of our investigation is the use of
an integrated comprehensive database, with primary data collected by professional
herpetologists from previously non-studied regions. Here, we aimed to analyze
the invasion ecology of this alien reptile in dierent parts of Eurasia, establishing
foundations for the verication of its invasive status and for an update of current
biosecurity approaches.
Andrey N. Reshetnikov et al. / NeoBiota 81: 91–127 (2023)
96
Materials and methods
Data collection
For assessing the current distribution, the veried original records of the red-eared slider
from 236 geographic localities were collected by the authors of this paper during their
eld inspections of water bodies in dierent regions of Eurasia in 2002–2020. Addition-
ally, 1241 relevant records from 1968–2020 were obtained from scientic papers (Suppl.
material 1), however 99.4% of these literature records are from 1990 and later, and
96.1% are from 2000 and later. All original data were subjected to rigorous verication.
In doubtful cases, i.e., without georeferenced location or exact identication of terrapins
by authors of observations, we requested and analyzed the coordinates of the localities,
and photos with details of head and neck coloration for correct identication. e iden-
tity of 167 inconclusive cases (not included in the above-mentioned numbers) was not
conrmed and they were therefore not included in the analysis. We also used two datasets
(for Europe and Asia) from the Global Biodiversity Information Facility (GBIF; www.
gbif.org) with records from 1978–2020. Assuming red-eared slider is an invasive taxon
with described remarkable impact on native species (Cadi et al. 2004; Perez-Santigosa et
al. 2008), and keeping in mind the absence of data on its impacts for the majority of the
georeferenced records, we analyzed all above-mentioned data regardless of impact. e
data were structured into categories depending on the source of data (original/literature/
GBIF) and identication level (species/subspecies). We did not include in the analysis the
available data on the presence of red-eared sliders in open water bodies on territories of
zoological parks (e.g., Rupperswil, Klagenfurt, Belgrade, Soa, Odessa, Moscow, Rostov-
on-Don, Barnaul, Singapore, Izmir, Istanbul, Mersin, Antalya) because of likely manage-
ment and care by sta (i.e., articial wintering of adult terrapins, special conditions for
egg incubation), but we used data from other urban parks. e original and literature re-
cords of the red-eared slider were distributed as follows: 713 in Europe, 589 in East Asia,
21 in North Asia, 61 in West Asia, 4 in Central Asia, 50 in South Asia, 39 in Southeast
Asia (see Suppl. material 2 for delineation of the continent). e database of original and
literature records is available in Suppl. material 3. e data from GBIF represented 5967
records from Europe and 31 records from Asia. Altogether, 1477 original/literature re-
cords and 5998 records from GBIF of T. s. elegans were included in the analysis (Fig. 1a).
Terminology
We used earlier suggested terms (Reshetnikov 2013) for discussion of the invasion pro-
cess: a. initial introduction; b. center (source) of the secondary distribution, i.e., the region
invaded by the alien species around the point of initial introduction serving as a source
for further expansion; c. invaded subrange, i.e., part of the invaded range assumed to
have originated from a single or a limited number of initial introductions, geographically
separated from other invaded subranges, which may be temporally separated and later
merged. Commonly, these processes are identied through the spatio-temporal analysis
of records but additional tools, such as molecular-genetic methods, are also important.
e paradox of a popular pet terrapin expansion in Eurasia 97
Figure 1. e 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 1); 2 (red circles)
– original records; 3 (blue circles) – records from GBIF.org (12 September 2020) GBIF Occurrence Down-
load https://doi.org/10.15468/dl.4qk7b3; https://doi.org/10.15468/dl.tppua3. e layers are located from
1 (above) to 3 (below) b spatio-temporal dynamics of records: 1 (black circles) – records of 1968–1989;
2 (green circles) – records of 1990–1999; 3 (blue circles) – records of 2000–2009; 4 (red circles) – records
of 2010–2020. e layers are located from 1 (above) to 4 (below); c the ecology: 1 (red circles with dot)
– records of established populations; 2 (red circles) – conrmed successful reproduction; 3 (red triangles) –
unsuccessful reproduction attempts; 4 (blue circles) – conrmed successful overwintering; 5 (green circles)
– records without information on ecology. e layers are located from 1 (above) to 5 (below).
Andrey N. Reshetnikov et al. / NeoBiota 81: 91–127 (2023)
98
Habitats, number of terrapins per water body, body sizes and ecology
We used all available georeferenced data (1968–2020) to understand the invasion ecol-
ogy 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). e
proportion of records with appropriate data are presented for each part of Eurasia
separately in Table 1.
Table 1. 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 individu-
als 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. mate-
rial 4. To assess the degree of synanthropy we used the above-mentioned data on habitats
as continuing transition from habitats outside human settlements (lowest synanthropy)
to recreational parks (highest synanthropization). When calculating relationships with
sizes, we ignored scores “6” and “7” (“adults”, “all sizes”) as well as cases with several dier-
ent sizes in the same water body. To build a histogram with body sizes, we included cases
with several dierent sizes in the same water body (e.g., 1, 3 or 2, 3, 4); they were counted
as separate cases of observations. erefore, contrary to correlation analysis, the histogram
with size classes represents analysis of cases of observations but not of water bodies. For
assessment of the degree of reproduction success, we used data on ecology (see Suppl.
material 4) after excluding score “1” (“casual records”). erefore, the reproduction scale
represents a continuum from just successful overwintering to established populations.
Species distribution models
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 pop-
ulation establishment (SDM1); (b) the potential range of successful overwintering as a
probable area of long-term survival of released individuals (SDM2). e 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 ar-
eas for MaxEnt models; (iv) determination of MaxEnt model parameters; (v) building
SDMs using MaxEnt.
e paradox of a popular pet terrapin expansion in Eurasia 99
i. Preparation of vector and raster layers. Vector layers of occurrence records were
created in ArcGis 10.6.1 (Environmental Systems Research Institute 2020) using the
full number of available records (9204 records: 1729 in the native and 7475 in Eurasian
invasive parts of the slider range). Bioclimatic variables (all 19) were obtained from the
WorldClim 2.1 dataset (Hijmans et al. 2005). In addition to this dataset, we also analyzed
16 predictor variables from the ENVIREM dataset (Title and Bemmels 2018), many of
which are related to the ecology of the terrapin under study. us, we created raster lay-
ers for 35 environmental variables at a spatial resolution of 2.5 arc minutes (~5 km2) for
further analysis. is stage was common for both (SDM1 and SDM2) models.
ii. inning of environmental variables and georeferenced records. We tested
for mulicollinearity amongst the potential predictor variables using two methods: the
Pearson correlation coecient, with a threshold value of > 0.75; and the variation
ination factor (VIF), with a threshold value of > 10 (Hair et al. 1995). e corSelect
function in the fuzzySim package (Barbosa 2015) was used for these analyses. Based
on these results, and the ecological requirements of the red-eared slider, we selected
four predictor variables that were used in the SDMs. e selected four variables, their
descriptions and links to slider ecology are as follows:
• BIO10 (dened as the mean temperature of the warmest quarter). is vari-
able represents the availability of thermal energy, particularly for feeding activity, and
was included because the northern distribution of red-eared sliders may be limited by
low summer temperatures. is species requires water temperatures higher than 10 °C
for the activation of feeding behavior, while the optimal soil temperature for embry-
onic development of eggs is 26–32 °C (Parmenter 1980).
• growingDegDays0 (dened as the sum of mean monthly temperature for
months with mean temperature greater than 0 °C, multiplied by the number of days
in that month). is variable reects the duration of the ice-covered period, i.e., time
without access to air oxygen. Red-eared sliders are assumed to have limited ability for
long-term survival under anoxic conditions (Ultsch 2006).
• BIO18 (dened as levels of precipitation during the warmest quarter). is
variable may be important for humidity-dependent embryonic development of skin-
shelled eggs of red-eared sliders (Tucker et al. 1998).
• climaticMoistureIndex (dened as a metric of relative wetness and aridity).
is variable is related to water availability and hence is a key factor for the stability of
aquatic habitats (shallow water bodies), which may shrink during summer.
In our case, the maximum Pearson coecient 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 spin package in R (Aiello-Lammens et al.
2015) to subsample the data ten times, using ten thinning parameters – the records
were separated by distances of 10–100 km in intervals of 10 km. en the ten
datasets were subjected to a cluster analysis using the average nearest neighbor index
(ANNI) in ArcGis 10.6.1 (Environmental Systems Research Institute 2020). After this
Andrey N. Reshetnikov et al. / NeoBiota 81: 91–127 (2023)
100
analysis, we chose the set of georeferenced records for which ANNI=1. As a result of
this approach, we obtained a reduced dataset which was used for preparation of two
datasets (DS1, DS2) for creating two bioclimatic models (SDM1, SDM2) accordingly
(Suppl. material 6): the potential range of successful reproduction as an assessment
of the probable area of population establishment (SDM1); the potential range of
successful overwintering as a probable area of long-term survival of released individuals
(SDM2). e rst model was built based on georeferenced records (DS1) from the
native range of the species in North America, taken from the International database
GBIF (n=373 from GBIF.org (29 July 2020) GBIF Occurrence Download https://doi.
org/10.15468/dl.d88pay; we veried this dataset by comparing with the native range of
T. s. elegans reported in Rhodin et al. 2017) and Eurasian original and literature records
of successful reproduction and established populations (n=98). e second model, i.e.,
wintering range, was based on DS2 which included the above-mentioned datasets, with
the addition of records of conrmed successful overwintering within Eurasia (n=124).
iii. Selection of background areas for MaxEnt models. We used the conven-
tional choice of background localities from the presence region, here dened as the
convex polygon, to build the two models (Rodda et al. 2011). However, the conven-
tional choice of background localities in convex polygon may have some limitations
as this minimizes the contrast between presence and absence, so we employed the
recommendations presented in previous literature (Lobo et al. 2008; Lobo et al. 2010).
ese studies suggest selecting backgrounds from areas that are immediately adjacent
to occupied habitats but are known to be unoccupied. For this reason, we combined
convex polygons located in North America, southern Europe, East Asia, and Southeast
Asia, which included appropriate georeferenced records. Background areas for the two
models are presented in Suppl. material 6.
iv. Determination of MaxEnt model parameters. Although the SDMs built
with MaxEnt (MaxEnt.jar; Dismo) (Phillips and Dudík 2008; Hijmans et al. 2017)
using default parameters were based on extensive empirical material, some studies
have shown that they can be inecient (e.g., Muscarella et al. 2014). For this reason,
we determined the optimal MaxEnt model parameters for each type of model using
the AICc information criterion in the ENMeval R package (Muscarella et al. 2014).
ENMeval applies three threshold-independent evaluation metrics: AUCTest, AUCDi,
and the size-corrected Akaike information criterion (AICc). AUCTest is a metric that
measures the discriminative ability of an SDM using georeferenced records that
were not used when the model was built. AUCDi is the dierence between the AUC
calculated from the AUCTrain training sample and AUCTest. is metric (AUCDi) is
a measure of model overtraining. AICc, adjusted for small sample size, reects the
degree of t and complexity (Muscarella et al. 2014; Guisan et al. 2017; Title and
Bemmels 2018). e ENMeval package creates a number of MaxEnt models for each
dataset using dierent regularization multiplier (RM) values and feature classes (FC),
compares them using the AICc criterion and chooses the most appropriate model. is
package typically selects a model that is less complex than the default model adopted
by MaxEnt, with acceptable AUCTrain and AUCDi metrics (Halvorsen et al. 2016; Title
and Bemmels 2018). Although we did not nd any general trends in the selection of
e paradox of a popular pet terrapin expansion in Eurasia 101
FC, the FCs selected using the AICc models had higher RM values than the default
value of 1.0 (Suppl. material 7). As a result, the following parameters were chosen for
SDM1: feature classes (L = linear, Q = quadratic), and RM=4.0. For SDM2- feature
classes (L = linear, Q = quadratic, H = hinge, P =product and T = threshold), and
RM=4.0 (see Suppl. material 7)
v. Building SDMs using MaxEnt. Species distribution models were built us-
ing the maximum entropy method by MaxEnt 3.4.1 with optimal MaxEnt param-
eters (Hijmans et al. 2017). When training the models, we used occurrence records
and background areas as presented in Suppl. material 6. We used a ‘sre’ strategy for
the random generation of the background (pseudo-absence) (PA) points using the
Biomod v.2.0 R package. e number of PA points generated (as recommended by
Barbet-Massin et al. 2012) was according to the number (N) of georeferenced records
(if N ≤ 1000 then 1000 points were selected, otherwise 10,000 points were selected).
At the next stage, we projected the MaxEnt models with optimal parameters onto the
territory of Eurasia. Final versions of these models were built as a result of 10 MaxEnt
runs to randomly select test and training georeferenced records. In all MaxEnt runs,
80% of the records were used as training samples while 20% served as test samples. We
used the Boyce index (Bind) to assess model performance (Boyce et al. 2002; Di Cola
et al. 2017), with the help of the EcoSpat R package (Di Cola et al. 2017). e Boyce
index lacks the drawbacks present in the AUC index (Lobo et al. 2008; Guisan et al.
2017; Petrosyan et al. 2020).
Analysis of niches
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. ese parts of the range were selected because of sucient records of four ecologi-
cal characteristics: conrmed successful overwintering, unsuccessful reproduction at-
tempts, conrmed successful reproduction, and established populations. Comparative
analysis was performed using GLM ANOVA (see section Statistics) based on raw val-
ues of ecologically important predictor variables (BIO10, BIO18, growingDegDays0,
climaticMoistureIndex the same as used for the SDMs – see the methodology above).
Statistics
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 cor-
relation coecient 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
Andrey N. Reshetnikov et al. / NeoBiota 81: 91–127 (2023)
102
the chi-square statistical test and then the Tukey Post hoc test (Zar 2010). In addition,
we also used the Shannon’s index to assess body size diversity in these parts of the
range. A comparative analysis of Shannon’s indices for size diversity was made using
the test proposed by Hutcheson (Magurran 1988).
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., xed factor models. In the rst ANOVA model we used
the factor “geographic region” and compared species niche centroids (means of predictor
variables) in dierent 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 mod-
els, the factor “establishment success” was used, consisting of four levels of reproductive/
establishment status (see above). is analysis is important to identify the range of en-
vironmental parameters favorable for successful reproduction. If an analysis of variance
with xed eects showed a signicant dierence in the level of factors, a test of multiple
comparison, the Post hoc Tukey HSD was used to determine which levels of the factor
diered from each other. For multiple comparisons with unequal variances according
to Leuven’s test, the Tukey-Cramer test with Welch’s modication was used (Zar 2010).
Prior to the analysis, all data were Log-transformed to achieve normal distribution of
the GLM ANOVA residuals. is additional analysis is important because it allows us
to test the validity of GLM ANOVA results using non-transformed data with residuals
that dier from the normal distribution, as recommended in the literature (Zar 2010).
Statistical analysis was performed using basic and special packages in the R lan-
guage in RStudio Version 1.2.5033 (RStudio Team 2020). We used MaxEnt.jar and
a set of R packages spin (Aiello-Lammens et al. 2015), ENMeval (Muscarella et al.
2014), EcoSpat (Di Cola et al. 2017), Biomod2 (uiller et al. 2021), Raster (Hijmans
et al. 2022), Dismo (Hijmans et al. 2017), fuzzySim (Barbosa 2015) in RStudio Ver-
sion 1.2.5033 (RStudio Team 2020) to build SDM models. In addition, we also used
ArcGis 10.6.1 (Environmental Systems Research Institute 2020) to prepare raster layers
of predictor variables, analyze the average nearest neighbor index, and visualize SDMs.
Results
Spatio-temporal dynamics and current occurrence range in Eurasia
Records from 1968–1989 fall into countries in Europe, West Asia, and East Asia.
e earliest records were reported from the Czech Republic from 1968, southern
Japanese islands from 1972, Israel from 1975, the Netherlands from 1980, and Bel-
gium 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, Is-
rael, Japan, ailand, Vietnam, Republic of Korea and the Taiwan Island). By 2010
e paradox of a popular pet terrapin expansion in Eurasia 103
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. 1b.
Synanthropy
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. 2a). In West Asia, with 51 appropriate observations, records in human settle-
ments reach 86.3% (Fig. 2a). In Europe, synanthropy of the red-eared slider is more
typical for eastern regions (see Suppl. material 5). Despite the general assessment that
synanthropy did not correlate to latitude (see Suppl. material 5), records of the terrapin
outside urban territories and rural settlements (score 1) highlighted a negative correla-
tion with latitude values in Europe (R = –0.10; t(n–2) = –2.41; N = 587; p<0.05) and
a positive correlation with reproduction success (R = 0.20; t(n-2) = 2.36; N = 135;
p<0.05). In Europe, more synanthropic groups of terrapins are more abundant (higher
number of individuals per water body), and portion of registered synanthropic groups
has increased over the years. In East Asia, synanthropy is less common in southern
regions and, similarly to Europe, has increased over the years. In West Asia, more
synanthropic groups are more abundant (see Suppl. material 5).
Distribution of red-eared sliders among the three types of habitats does not dif-
fer between the European and East Asian parts of the range, but habitat distribution
in both regions signicantly diere from habitat distribution in West Asia (Fig. 3).
Remarkably, in all parts of the studied range, the proportion of records in the second
habitat, i.e., records located in water bodies within human settlements but outside
recreational areas, is signicantly greater than that of habitats 1 and 3, sites outside
human settlements and public parks (Fig. 3). In West Asia, the studied terrapin is
found signicantly more often in parks and other recreational areas (Fig. 3) compared
with Europe and East Asia. e proportion of records in habitat 2 (Fig. 3) in West
Asia is signicantly less than in Europe and East Asia. e proportion of records in
nature environments (habitat 1), i.e., outside human settlements, does not dier in
the three regions (p = 0.06): 16, 14 and 17.5% in Europe, West Asia and East Asia,
respectively (Fig. 3).
Number of terrapins per water body
e three regions with the highest number of observations, Europe, West Asia, and
East Asia (Fig. 1a), have a remarkably higher percentage of water bodies with more
than one red-eared slider individual per aquatic site compared with other parts of
Eurasia: (χ2= 100.6, df = 6, P << 0.001) (Fig. 2b). e highest portion of such wa-
ter bodies was observed in East Asia (72.9%); here, the proportion of these water
bodies was signicantly higher than in Europe, 43.0% (Z = 8.5, P << 0.01). e
mean number of slider individuals per aquatic site was 23.2±9.6 (1–4288; n=490)
Andrey N. Reshetnikov et al. / NeoBiota 81: 91–127 (2023)
104
for Europe; 10.1±2.6 (1–98; n=57) for West Asia; 61.8±31.9 (1–10000; n=318)
for East Asia (observations with an estimated number of “several individuals” were
excluded from this calculation). Proportion of larger groups increased over the years
in Europe (see Suppl. material 5). Here, the greatest numbers (>200 ind. per water
body; 1186.4±537.1 (250–4288; n=7)) were reported in the 2000s in Spain (re-
gions of Doñana National Park and Valencia (Perez-Santigosa et al. 2008; Sancho
and Lacomba 2013). In East Asia, the greatest number (>200 ind.; 1425.4±860.6
(212–10000; n=11)) were noted in several regions of Japan and China (e.g., Tani-
guchi et al. 2017; Gong et al. 2018). We are not aware of such large groups of
red-eared sliders in other parts of Eurasia. Ignoring these 18 extra-populated water
bodies, the mean number of individuals in groups was 15.4±2.5 (2–191; n=485)
for Europe, 15.8±4.0 (2–98; n=35) for West Asia and 17.6±1.9 (2–200; n=220)
for East Asia. e number of individuals per water body in Europe correlated nega-
tively with latitude in the original/literature dataset even after excluding seven extra-
populated (>200 ind.) water bodies in southern regions (R = –0.13; t(N–2)= –2.83;
N = 485; p<0.01). Such correlation is absent for water bodies in West Asia and East
Asia (R = –0.22; t(N–2)= –1.66; N = 57; NS and R = 0.02; t(N–2)=0.33; N = 305;
NS, respectively). However, the number of individuals correlates negatively with
longitude in West Asia (R = –0.29; t(N–2)= –2.22; N = 57; p<0.05) and positively
Figure 2. Ecological characteristics (left axis, %) and numbers of observations (at the tops of columns) of
the red-eared slider Trachemys scripta elegans in dierent 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.
e paradox of a popular pet terrapin expansion in Eurasia 105
in East Asia (R = 0.19; t(N–2)=–3.36; N = 305; p<0.001) reecting association with
coastal regions, the Mediterranean coast in West Asia and the Pacic (seas of Pacic
Ocean) coast in China.
Body sizes
Diversity and proportions of observations (not water bodies) of various size classes
of red-eared slider in parts of Eurasia are presented at Fig. 2c. Below we discuss
an assessment of the proportions of water bodies (%) inhabited by individuals of
dierent size classes. Small individuals, with carapace length ≤ 10cm, are detected
rarely: in 8.0, 12.5 and 4.6% of water bodies of Europe, West Asia, and East Asia,
respectively. Including the category “all sizes”, these percentages are 20.8, 33.3 and
70.4%, respectively. Big individuals with carapace length > 15cm were noted in
aquatic sites of Europe, West Asia, and East Asia in 31.8, 52.1 and 17.5% or 88.1,
85.4 and 91.2% when including categories “adults” and “all sizes”. Very big ter-
rapins (> 20cm) were conrmed in 14.8, 4.2 and 13.7% of areas, respectively. In
Europe, the occurrence of small individuals (≤ 10cm; scores 1, 2, 7) negatively cor-
related with latitude (R = –0.24; t(N–2)= –3.72; N = 236; p<0.001), longitude
(R = –0.25; t(N–2)= –4.00; N = 236; p<0.001), positively correlates with number
per water body (R = 0.57; t(N–2)= 10.27; N = 215; p<0.001) whereas occurrence
of very big individuals (score 5) positively correlated with latitude (R = 0.17; t(N–
2)=2.72; N = 236; p<0.01) and negatively correlates with longitude (R = –0.20;
Figure 3. Comparison of the distribution of red-eared sliders among habitats in three dierent parts of
the Eurasian invaded range. See details of habitat coding in Suppl. material 4. Whiskers show 95% Wald’s
condence intervals. A multiple comparison of proportions of the same habitat types in dierent parts
of the invaded range was performed using the Chi-square (Biotope 1: 12.5, df = 2, p = 0.001; Biotope 2:
1378.8; df = 2, p < 0.001; Biotope 3: 5.8, df = 2, p = 0.06) and Tukey’s Post hoc tests. Signicant dier-
ences between proportions of the same biotopes in dierent parts of the range are marked by *.
Andrey N. Reshetnikov et al. / NeoBiota 81: 91–127 (2023)
106
t(N–2)= –3.09; N = 236; p<0.01). In West Asia, the occurrence of small individuals
did not correlate with latitude or longitude (R = 0.16; t(N–2)=1.16; N = 48; NS
and R = 0.16; t(N–2)=1.09; N = 48; NS); in East Asia, this size did not correlate
with latitude (R = 0.06; t(N–2)=–0.20; N = 240; NS) but positively correlates with
longitude R = 0.20; t(N–2)=3.18; N = 240; p<0.01). erefore, occurrence of small-
sized individuals positively correlates with coastal areas. Interestingly, in West Asia,
registration of bigger individuals is more typical for water bodies with large groups
of red-eared sliders and has increased over time (see Suppl. material 5).
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. 4). Hutcheson’s test suggests the following ranked
series for this index: H (East Asia) (t = 51.1; df = 220; p << 0.05) >> H (Europe)
(t = 8.87; df = 114; p << 0.05) >> H (West Asia). Although data on the reproductive
status in the studied parts of the range are limited, nevertheless, high H index values
in East Asia and Europe suggest high size diversity with a sucient number of both
young and mature individuals in these parts of the range for the establishment of
populations, if climatic conditions are appropriate.
Ecology
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,
Figure 4. Shannon’s index of body size diversity (H) for three dierent parts of the Eurasian invaded
range. Whiskers show 95% Hutcheson’s condence interval.
e paradox of a popular pet terrapin expansion in Eurasia 107
whereas successful reproduction and even establishment of populations is reported
from southern Europe, West Asia, East Asia, and Southeast Asia (Figs 1c, 2d). In Eu-
ropean water bodies, successful wintering depended negatively on latitude (R = –0.23;
t(N–2)=–6.22; N = 671; p<0.001; observations of successful reproduction and estab-
lishment of populations were also regarded as wintering points and included in the
analysis here and below) and did not correlate with longitude (R = 0.03; t(N–2)=0.68;
N = 671; NS) whereas successful wintering in West Asia and East Asia did not depend
on latitude (R = 0.05; t(N–2)=0.42; N = 59; NS and R = 0.01; t(N–2)= 0.25; N = 586;
NS, respectively). We found such a correlation with longitude for the water bodies
of West Asia (R = –0.49; t(N–2)= –4.24; N = 59; p<0.0) and East Asia (R = 0.12;
t(N–2)= 2.93; N = 586; p<0.01). We regarded the relationship between mortality dur-
ing wintering and latitude using the example of the European part of Russia, a region
with a remarkable climatic gradient of thermal conditions. Here, winter mortality was
reported for 9.5% of water bodies. We did not nd correlations between mortality
events and latitude (R = 0.00; t(N–2) = 0.03; N = 73; NS) as dead individuals were
registered in both northern (e.g., Saint-Petersburg, Moscow) and southern regions
(e.g., Stavropol and Krasnodar territories, Voronezh province of Russia).
In Europe, reproduction is more eective in southwestern regions and positively
correlates with terrapin abundance (see Suppl. material 5). In East Asia, reproduction
is more successful in the eastern part. e registrations of reproduction have decreased
over the years in both Europe and East Asia (see Suppl. material 5). e potential range
of reproducing populations of the red-eared slider, as well as the potential range of suc-
cessful wintering, are presented in Figs 5a, b.
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 tem-
perature above 0 °C (SigmaT = 7.78 * 104 ± 3207 °C) (Fig. 6). Some niche centroids in
West Asia occupy an intermediate position (T = 23.4 ± 0.49 °C; n = 31; SigmaT = 5.868
* 104 ± 3408 °C; n = 31) compared to centroids in Europe and East Asia. e moisture
index in the West Asian part of the range (Mi = -0.33 ± 0.03; n = 31) is signicantly
lower than in East Asia, but does not dier from Europe (Mi = -0.27 ± 0.02, n = 75).
Concerning precipitation in the warm season, the niche of the red-eared slider in West
Asia is characterized by the lowest precipitation (W = 82.3 ± 16.7 mm; n = 31). e
centroids of temperature (T = 19.3 ± 0.32 °C, n = 75) and the sum of temperatures
(SigmaT = 3.671 * 104 ± 2191 °C, n = 75) in Europe are characterized by the lowest
values, do not dier in the humidity index from the West Asian part of the range, and
occupy an intermediate position in terms of precipitation in the warm season of the
year. e centroids of niches in East Asia dier signicantly from two other analyzed
parts of the range for all studied predictor variables (Fig. 6). Comparison of the mean
values of the Log-transformed predictor variables using GLM ANOVA is presented
in Suppl. material 8: g. S4. It can be seen that Fig. 6 and Suppl. material 8: g. S4
similarly display niche centroid positions across all predictor variables. e normal
Andrey N. Reshetnikov et al. / NeoBiota 81: 91–127 (2023)
108
distribution of GLM ANOVA residuals after Log-transformation for all variables sug-
gests that conclusions regarding the signicance of the centroid dierence, established
without data transformation, are correct.
A comparative analysis of the parameters of reproductive eorts in Eurasia showed
that centroids 2 and 3 (wintering and egg laying) signicantly dier from 4 and 5
(successful reproduction and establishment of populations) (Fig. 7). We combined
centroids of 2 and 3 and presented them as level I and combined 4 and 5 as level
II. e appropriate mean values and ranges of values for level I (n = 100) in Eura-
sia are as follows: T = 20.6 (range 19.1–21.21) °C; W = 298.5 (206.3–390.7) mm;
Figure 5. 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 Mod-
el 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. 5a with the addition of records with conrmed successful wintering within Eurasia
(which are shown by pink points).
e paradox of a popular pet terrapin expansion in Eurasia 109
Mi = -0.17 (-0.31 – -0.04); SigmaT = 4.152*104 (3.22*104–5.084*104) °C and for
level II (n = 41) are: T = 25.5 (24.4–26.7) °C; W=521.3 (410.2–631.0) mm; Mi = 0.15
(0.08–0.3); SigmaT = 7.294*104 (6.185*104–8.404*104) °C. A comparative analysis
of the parameters of reproductive eorts in Eurasia with Log-transformed data is pre-
sented in Suppl. material 8: g. S4. Importantly, the results of comparing the niche
centroids did not dier regardless of whether the original data are Log-transformed or
not. Since the residuals of the GLM ANOVA models after Log-transformation of the
predictor variables did not dier from the normal distribution, we therefore limited
our comparison to mean values only.
Discussion
Spatio-temporal dynamics
e 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 (Moravec and Široký 2006), and East Asia (Okinawa
Figure 6. Comparison of mean values (± 95% Tukey HSD condence intervals) of the main predictor
variables of terrapin habitats in dierent parts of the invaded range. e results of one factor ANOVA
based on General Linear Model are presented. e GLM ANOVA tested the main eects 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 eects). Signicant dierences of means
according to Post hoc Tukey HSD test are marked by *. Absence of signicant dierences is marked as
NS, i.e., values for Europe and West Asia do not dier from each other on Fig. 6c. Records with ecological
characteristics 2–5 (see Methods) were used (so, we ignored casual records for this analysis).
Andrey N. Reshetnikov et al. / NeoBiota 81: 91–127 (2023)
110
Island, Japan), with detection in 1972 (Shimazu 2015). Soon after, this alien was also
rst detected in West Asia (Bethlehem, Israel) in 1975 (Bouskila 1986). Up to the
beginning of 21st century, outdoor occurrence of the species under study was restricted
mainly to Europe and East Asia, with less frequent reports in West Asia and Southeast
Asia (Fig. 1b). Contrary to the invasion histories of some “classical” invaders such as
the insect Agrilus planipennis or sh Perccottus glenii (e.g., Reshetnikov and Ficetola
2011; Orlova-Bienkowskaja et al. 2020), colonization by the red-eared slider did not
have a limited number of initial introductions which became sources of secondary
distribution with the potential establishment of invaded subranges. e geographical
expansion of this reptile was driven by massive propagule pressure in dierent regions
over the huge territory of Eurasia. Nevertheless, Europe and East Asia were the regions
with earliest and greatest dissemination compared with other parts of the continent
(Fig. 1b). To date, this terrapin species is present in almost all countries of Eurasia
(Fig. 1a). It has been reported from 68 Eurasian countries. e original list of Eurasian
countries colonized by red-eared slider is available in the Suppl. material 9.
Figure 7. Comparison of mean values (± 95% Tukey HSD condence intervals) of main predictor
variables of terrapin habitats for records with dierent ecological/reproductive statuses. e results of one
factor ANOVA based on General Linear Model (GLM) are presented. e GLM ANOVA tested the main
eects of reproduction status (where 2 is conrmed successful overwintering; 3 is unsuccessful reproduc-
tion attempts, 4 is conrmed 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 eects). Statistically signicant dierences of means according to
Post hoc Tukey HSD test between 4 and 2, 3 (separately) is marked by *; statistically signicant dierences
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. e same is true for 4 and 5.
e paradox of a popular pet terrapin expansion in Eurasia 111
Invasion ecology
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 dierent parts of Eurasia. We
found that the ecological niche of reproductive groups of the red-eared slider in East
Asia diers from those in Europe and West Asia in terms of thermal energy and mois-
ture (Fig. 6). is may be explained by the absence of the whole range of appropriate
favorable environmental conditions in Europe and West Asia. Breeding groups of this
invader are likely to occupy habitats with more favorable climatic conditions in East
Asia, with higher temperature and humidity compared with other parts of Eurasia (Fig.
6). Despite the absence of appropriate records of reproductive success, our modelling
conrms the existence of large territories favorable for reproduction in non-coastal
regions of China and Azerbaijan, and southern Turkey, as well as limited regions of
several other countries, including Kazakhstan (south), Iran (north), India, Nepal and
others (Fig. 5).
Importantly, the red-eared slider inhabits mainly urban and rural environments
(Fig. 2d) because the principal invasion vector is pet release (Semenov 2010; Banha
et al. 2017). It is not surprising that synanthropic groups of this terrapin are more
abundant, as it has been shown for Europe and West Asia. However, the distribution
of red-eared sliders is not limited by territories of human settlements, where this ter-
rapin is often used for decoration of ponds. is invader has already been detected in
natural environments, i.e., outside human settlements, in most parts of Eurasia (Fig.
2a). In Europe and East Asia, the proportion of records in natural habitats reaches
16–17%. In West Asia, records in natural water bodies amount 13.7%. is reects
the unavoidable dispersion of these animals from points of initial introductions (e.g.,
urban and rural ponds) to other places. Pet terrapins can migrate to natural habitats
both through the hydrological network and over land; however, at least in some cases,
they were introduced directly into nature (e.g., Doñana National Park, Perez-Santigosa
et al. 2008).
Recorded red-eared slider numbers may entirely (in regions without reproduction)
or partly (in regions with reproduction) reect past human activities, i.e., accumula-
tion of human-released slider individuals, a phenomenon dened as “invasion debt”
(Essl et al. 2011). Commonly, aquatic sites with red-eared sliders have one terrapin
individual per water body, however the number varies and mean values are tens of in-
dividuals for dierent parts of Eurasia, with the highest abundance in East Asia, where
the mean value is 62 individuals per water body. High numbers and biomass of this
alien hydrobiont produces risks for native freshwater ecosystems (Cadi and Joly 2004;
Lee et al. 2016; Salerno and van den Burg 2021). In Eurasia, the number of sliders
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112
may reach thousands of individuals per aquatic site (Perez-Santigosa et al. 2008; San-
cho and Lacomba 2013; Taniguchi et al. 2017; Gong et al. 2018). erefore, this alien
reptile became a target of eradication campaigns in this region from the early 2000s
(e.g., Sancho and Lacomba 2013). However, despite possible local success, our review
did not reveal any signs of decrease in terrapin abundance over the years, or signs of
decreasing geographical range on the all-Eurasian scale (see Suppl. material 5; Fig. 1b).
Our results show a higher density of records of the slider in Europe and East Asia
(Fig. 1b). e density of records may correlate positively with the density of human
population (Banha et al. 2017). Propagule pressure (the number of release events) is
often positively correlated with human population density, whereas survival and repro-
ductive success of terrapins depends mainly on climate conditions, i.e., fundamental
niche. erefore, both climatic and anthropic factors are important to this terrapin
for invasion. Analyzing invasion ecology, we found that many characteristics of inva-
sion success (e.g., higher portion of inhabited natural water bodies, higher number of
individuals per water body, successful overwintering, presence of juvenile individuals,
successful reproduction and establishment of populations) tend to be present in coastal
regions, such as the Mediterranean coast of southern Europe, the western part of West
Asia, the Pacic coast of East Asia and islands. e coastal regions could have milder
thermic and more favorable humidity regimes, which are important for the reproduc-
tion of this reptile.
Reproductive success depends on several key environmental parameters (Fig. 7).
Assessing bioclimatic dierences between presence and reproduction occurrence is im-
portant (Ficetola et al. 2009; Heidy Kikillus et al. 2010). For example, despite a great
number of occurrence records in Europe, the establishment of self-sustained popula-
tions of this terrapin has been proved only for southern regions of Europe in Spain,
Italy and southern France (Cadi et al. 2004; Perez-Santigosa et al. 2008; Ficetola et
al. 2009; Crescente et al. 2014). On the other hand, specialists report successful re-
production in a larger number of localities and do not exclude the possibility of es-
tablished populations in Portugal, Greece, Croatia, Slovenia, and Serbia, in locations
where a similar Mediterranean climate is prevalent (Bruekers et al. 2006; Đorđević
and Anđelković 2015; Standfuss et al. 2016; Koren et al. 2018; Martins et al. 2018;
Tzoras et al. 2018; Urošević et al. 2019; our data). Of course, some observed groups
of terrapin may be at dierent stages of invasion debt (Essl et al. 2011), with po-
tential establishment of populations in the future, after the accumulation of human-
released individuals of reproductive age and/or due to future climate alterations. In
regions with suboptimal climatic conditions, e.g., lowland territories of Switzerland
and Austria, and south Germany, the red-eared slider can also successfully reproduce
but more rarely, only in some very hot summers (Bringsøe 2001; Wüthrich 2004; Pieh
and Laufer 2006; Kleewein 2015; Schradin 2020). However, some above-mentioned
data originate from open areas of zoos (Wüthrich 2004; Kleewein 2015), not from
natural landscapes. Additionally, sometimes records of hatchlings from urban park
ponds (Bringsøe 2001; Pieh and Laufer 2006) are dicult to separate from bought
and released young-of-the-year juveniles (see facts and discussion in: Semenov 2010;
e paradox of a popular pet terrapin expansion in Eurasia 113
Ficetola et al. 2012). Registration of reproductive eorts, i.e., female egg-laying be-
havior, is the least informative ecological parameter because it characterizes neither
success of reproduction, nor physiological adaptation to local geographical conditions.
erefore, despite multiple registrations of unsuccessful reproduction eorts in some
more northern countries of Europe, e.g., Belgium, the Netherlands, Denmark, Czech
Republic, and Poland (Bringsøe 2001; Najbar 2001; Herder 2007; Brejcha et al. 2010;
Verbelen 2021), temperature conditions in those countries are, possibly, much less
favorable for successful development of embryos at the present time (Fig. 5a).
In the current analysis (Fig. 1c), the northernmost countries of successful repro-
duction of this reptile in West Asia and East Asia are Turkey, Japan and Republic of
Korea (Çiçek and Ayaz 2015; Taniguchi et al. 2017; Koo and Sung 2019). However,
climatic conditions of even some more southern regions of Asia seem to be unsuitable
for reproduction (Fig. 5a). We propose that cold mountain climates and lack of soil
humidity of some other regions inhibit reproduction of the studied reptile. Indeed,
the eggs of T. scripta have a skin envelope (Cagle 1944) and are less protected against
desiccation compared with hard-shell eggs of some other terrapins (Tucker et al. 1998).
Multi-year monitoring of groups of T. s. elegans individuals in an arid region do not
reveal successful development of naturally laid eggs under extremely dry conditions
(Drost et al. 2021), which further supports our hypothesis. Importantly, sex deter-
mination of embryos of the red-eared slider is temperature-dependent (Tucker et al.
2008). Only males appear under low incubation temperature; this feature is regarded
as a possible limitation for the establishment of populations in northern regions, with
insucient thermal conditions for the production of both sexes (Cadi and Joly 2004;
Heidy Kikillus et al. 2010). Additionally, red-eared sliders can inhabit thermal or heat-
ed water bodies with special microclimatic conditions and can benet from a higher
reproduction potential due to earlier maturation with greater body sizes, earlier start of
the nesting season and larger clutch sizes (ornhill 1982). For example, hatchlings of
T. s. elegans may be recorded in thermal springs (e.g., in Bulgaria, Kornilev et al. 2020)
outside areas of proven reproduction of this species. Among our dataset, the northern-
most records of this slider in North Asia (e.g., West Siberia and Kamchatka peninsula)
with rather severe climates are restricted to thermal reservoirs; however we have not
found conrmation of survival and reproductive success in those localities (Fig. 1c).
Paradoxical expansion without reproduction
e results of all the species distribution models have some dierences due to vari-
ations in datasets and climatic variable sets used. e calculated reproductive range
of the red-eared slider in Eurasia in our study (Fig. 5a) is based on the most compre-
hensive dataset and signicantly updates some earlier SDM prognoses of successful
reproduction for this terrapin (Rödder et al. 2009; Heidy Kikillus et al. 2010). For
instance, our model excludes England as an area favorable for reproduction. Analysis of
the literature indirectly suggests our model may be suitable because there have not yet
been reports conrming successful reproduction of the studied terrapin in England.
Andrey N. Reshetnikov et al. / NeoBiota 81: 91–127 (2023)
114
Nevertheless, current geographical occurrence of this terrapin (Fig. 1b) is not limited
to areas climatically suitable for successful reproduction (Fig. 5a). As the main inva-
sion vector and driver is pet releases (García-Díaz et al. 2015), the geography of initial
introductions does not depend on climate features. Despite the reproduction of this
terrapin being restricted to a few regions of Eurasia with comparatively high summer
temperatures and sucient air humidity (Fig. 1c), the released red-eared slider toler-
ates a wide range of temperatures and does not depend on air humidity around recipi-
ent water bodies. Individuals of this species activate their feeding behavior when water
temperature is above 10 °C (Parmenter 1980). Many lowland freshwater aquatic sites
of Eurasia reach such thermal conditions during summer. So, this terrapin becomes
included in the food webs of local ecosystems immediately after its release. It is as-
sumed that even a few big individuals of red-eared slider are capable of damaging low-
component ecosystems of small isolated water bodies like articial ponds (Semenov
2010). However, numbers of this invader often reach much higher values in Eurasian
water bodies (Fig. 2b). us, this reptile demonstrates wide expansion without estab-
lishment of populations. Recruitment of new individuals to “pseudopopulations” of
the red-eared slider takes place due to additional releases. Once released, individuals of
this terrapin may inhabit a water body up to 30–31 years (Frazer et al. 1990; Castanet
1994). As a result, despite the absence of reproduction in the most regions of Eurasia
(Fig. 5a), its occurrence area has enlarged considerably from the end of 1960s to the
late 2010s and presently covers a considerable portion of Eurasia (Fig. 1b).
Conditional invasion
e invasive status of a species assumes 1) naturalization, i.e., establishment of popu-
lations, and 2) remarkable negative impact on native species/ecosystems (Cadi et al.
2004; Standfuss et al. 2016). us, invasive status, sensu stricto, of this reptile is not
conrmed for the majority of Eurasian countries because established populations are
registered only in a few regions (Fig. 1c). However, keeping in mind its abnormally
high propagule pressure (García-Díaz et al. 2015), ability to survive under suboptimal
conditions (Willmore and Storey 1997), long life duration (Castanet 1994), increasing
numbers (without reproduction) due to progressive cases of releases and continuing
geographical expansion, this aquatic reptile has acquired invasive status without the
establishment of reproducing populations in areas where it can survive for more than
one year. Because of the lack of such an important feature as establishment of popula-
tions, this new type of invasion may be dened as a “conditional invasion”. is may
be applied to this reptile within the area of successful wintering excluding the area of
successful reproduction.
Wintering range as an important criterion for risk assessment
Successful wintering is registered for all parts of the continent (Figs 1c, 2d, 5b). e
only hitherto known conrmation of wintering in North Asia is restricted to the Far
e paradox of a popular pet terrapin expansion in Eurasia 115
East region of Russia, with its mild marine climate. We do not have conrmation of
successful overwintering in other regions of North Asia, which are characterized by a
severe continental climate with low winter temperatures. Interestingly, during severe
winters with subzero temperatures in southern regions, some individuals may die but
others can survive in the same water body (Stoyanov 2015). On the other hand, winter-
ing success can dier in dierent years depending on weather conditions (Reshetnikov
and Sokolov 2020). Climatic thresholds for successful wintering may be explained by
physiological restrictions. Red-eared sliders usually hibernate on the bottom of water
bodies and the aquatic environment reliably protects them against subzero tempera-
tures if a layer of water remains between the ice and bottom of the water body. Impor-
tantly, during hibernation, this terrapin can tolerate near-zero positive temperatures,
as well as considerable decit and even short-term absence of oxygen (Ultsch 2006);
therefore, this species is sometimes regarded as a facultative anaerobe (Willmore and
Storey 1997). eoretically, crucial criteria for survival may be: 1) duration of winter
ice-covering period because the red-eared slider does not survive if anoxic conditions
last longer than 44–50 days (Ultsch 2006); 2) number of days with water temperature
above 10 °C in the warm period, impacting the condition of the terrapin body prior to
wintering, e.g., lipid reserve, necessary for long hibernation without exogenous feed-
ing. Such body condition is dicult to reach in northern and mountainous regions
with a brief warm season, as well as in internal areas of the continent with a severe
continental climate. In such regions, climatic limitations of successful wintering may
be non-direct: this animal survives under low water temperatures, but is deprived of
the necessary physiological reserves that might prepare it to tolerate a prolonged period
of unfavorable conditions. Calculated limitations of wintering in some regions in the
south of Asia (Fig. 5b) are less understandable. eoretically, the main limiting factors
may be related to high temperatures and water decit, especially for vast arid areas of
Saudi Arabia, Yemen, Oman, Iraq and Afghanistan. However, we cannot exclude year-
round existence of the red-eared slider in oases with permanent aquatic sites.
We propose the “range of successful wintering” as a territory at risk for true inva-
sion as well as for conditional invasion. is 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.
Conclusions
e 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 prop-
agule pressure in dierent regions over its huge territory. e invasive range of this ter-
rapin enlarged gradually in Eurasia up to the beginning of the 2020s covering 68 Eura-
sian countries. In particular, we report original data outlining recent rst detections of
this alien terrapin in the following countries: Bangladesh, Georgia, Kazakhstan, Kyr-
gyzstan, Mongolia, Nepal, Pakistan, Tajikistan, as well as Russian Siberia (drainages of
Andrey N. Reshetnikov et al. / NeoBiota 81: 91–127 (2023)
116
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 ecol-
ogy conrm 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, occur-
rence of juvenile individuals, successful reproduction, and establishment of popula-
tions. Notably, a great number of established groups of this reptile in dierent 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. erefore, we highlight the signicance of the wintering range.
is range must be taken in account when planning measures of control of this invader
because non-reproducing groups of this terrapin may become a signicant component
of freshwater ecosystems with impact on native species. us, a cost-eective conserva-
tion strategy against the red-eared slider in large countries with a variety of climatic
zones may dier 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 reproduc-
tion and wintering. Nevertheless, some protective measures (i.e., banning of import
and trade) are eective 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.
Acknowledgements
We are thankful to subject editor K. Faulkner and two anonymous reviewers for valua-
ble 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 identication of terrapins observed in Essen. We greatly
appreciate A.V. Zhulina and A.A. Zibrova for their help with an illustration for a Sup-
pl. 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 10).
e work was partly supported by RSF, project no. 21-14-00123.
e paradox of a popular pet terrapin expansion in Eurasia 117
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Supplementary material 1
List of literature sources with records of red-eared slider in Eurasia
Authors: Andrey N. Reshetnikov et al.
Data type: Pdf le
Copyright notice: is dataset is made available under the Open Database License
(http://opendatacommons.org/licenses/odbl/1.0/). e Open Database License
(ODbL) is a license agreement intended to allow users to freely share, modify, and
use this Dataset while maintaining this same freedom for others, provided that the
original source and author(s) are credited.
Link: https://doi.org/10.3897/neobiota.81.90473.suppl1
e paradox of a popular pet terrapin expansion in Eurasia 125
Supplementary material 2
Eurasian subregions as accepted in the current article
Authors: Andrey N. Reshetnikov et al.
Data type: Pdf le
Copyright notice: is dataset is made available under the Open Database License
(http://opendatacommons.org/licenses/odbl/1.0/). e Open Database License
(ODbL) is a license agreement intended to allow users to freely share, modify, and
use this Dataset while maintaining this same freedom for others, provided that the
original source and author(s) are credited.
Link: https://doi.org/10.3897/neobiota.81.90473.suppl2
Supplementary material 3
Data base of georeferenced records of Trachemys scripta elegans in Eurasia
Authors: Andrey N. Reshetnikov et al.
Data type: xls le
Copyright notice: is dataset is made available under the Open Database License
(http://opendatacommons.org/licenses/odbl/1.0/). e Open Database License
(ODbL) is a license agreement intended to allow users to freely share, modify, and
use this Dataset while maintaining this same freedom for others, provided that the
original source and author(s) are credited.
Link: https://doi.org/10.3897/neobiota.81.90473.suppl3
Supplementary material 4
Coding of collected eld data
Authors: Andrey N. Reshetnikov et al.
Data type: Pdf le
Copyright notice: is dataset is made available under the Open Database License
(http://opendatacommons.org/licenses/odbl/1.0/). e Open Database License
(ODbL) is a license agreement intended to allow users to freely share, modify, and
use this Dataset while maintaining this same freedom for others, provided that the
original source and author(s) are credited.
Link: https://doi.org/10.3897/neobiota.81.90473.suppl4
Andrey N. Reshetnikov et al. / NeoBiota 81: 91–127 (2023)
126
Supplementary material 5
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)
Authors: Andrey N. Reshetnikov et al.
Data type: Pdf le
Copyright notice: is dataset is made available under the Open Database License
(http://opendatacommons.org/licenses/odbl/1.0/). e Open Database License
(ODbL) is a license agreement intended to allow users to freely share, modify, and
use this Dataset while maintaining this same freedom for others, provided that the
original source and author(s) are credited.
Link: https://doi.org/10.3897/neobiota.81.90473.suppl5
Supplementary material 6
Locations of the training areas based on the available occurrence records
Authors: Andrey N. Reshetnikov et al.
Data type: Pdf le
Copyright notice: is dataset is made available under the Open Database License
(http://opendatacommons.org/licenses/odbl/1.0/). e Open Database License
(ODbL) is a license agreement intended to allow users to freely share, modify, and
use this Dataset while maintaining this same freedom for others, provided that the
original source and author(s) are credited.
Link: https://doi.org/10.3897/neobiota.81.90473.suppl6
Supplementary material 7
Evaluation metrics for MaxEnt models made across a range of feature-class com-
binations and regularization multipliers
Authors: Andrey N. Reshetnikov et al.
Data type: Pdf le
Copyright notice: is dataset is made available under the Open Database License
(http://opendatacommons.org/licenses/odbl/1.0/). e Open Database License
(ODbL) is a license agreement intended to allow users to freely share, modify, and
use this Dataset while maintaining this same freedom for others, provided that the
original source and author(s) are credited.
Link: https://doi.org/10.3897/neobiota.81.90473.suppl7
e paradox of a popular pet terrapin expansion in Eurasia 127
Supplementary material 8
Comparison of mean values of the Log-transformed predictor variables
Authors: Andrey N. Reshetnikov et al.
Data type: Pdf le
Copyright notice: is dataset is made available under the Open Database License
(http://opendatacommons.org/licenses/odbl/1.0/). e Open Database License
(ODbL) is a license agreement intended to allow users to freely share, modify, and
use this Dataset while maintaining this same freedom for others, provided that the
original source and author(s) are credited.
Link: https://doi.org/10.3897/neobiota.81.90473.suppl8
Supplementary material 9
Original list of 68 Eurasian countries colonized by the red-eared slider Trachemys
scripta elegans
Authors: Andrey N. Reshetnikov et al.
Data type: Pdf le
Copyright notice: is dataset is made available under the Open Database License
(http://opendatacommons.org/licenses/odbl/1.0/). e Open Database License
(ODbL) is a license agreement intended to allow users to freely share, modify, and
use this Dataset while maintaining this same freedom for others, provided that the
original source and author(s) are credited.
Link: https://doi.org/10.3897/neobiota.81.90473.suppl9
Supplementary material 10
Additional list of 52 persons who kindly provided their observations of red-eared
sliders in open water bodies of Eurasia
Authors: Andrey N. Reshetnikov et al.
Data type: Pdf le
Copyright notice: is dataset is made available under the Open Database License
(http://opendatacommons.org/licenses/odbl/1.0/). e Open Database License
(ODbL) is a license agreement intended to allow users to freely share, modify, and
use this Dataset while maintaining this same freedom for others, provided that the
original source and author(s) are credited.
Link: https://doi.org/10.3897/neobiota.81.90473.suppl10
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