Journal for Nature Conservation 31 (2016) 22–28
Contents lists available at ScienceDirect
Journal for Nature Conservation
journal homepage: www.elsevier.de/jnc
Establishment risk and potential invasiveness of the selected exotic
amphibians from pet trade in the European Union
Oldřich Kopecký ∗ , Jiří Patoka, Lukáš Kalous
Department of Zoology and Fisheries, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Kamýcká 129, CZ-165
21, Praha 6—Suchdol, Czech Republic
a r t i c l e
i n f o
Article history:
Received 27 July 2015
Received in revised form 29 February 2016
Accepted 29 February 2016
Keywords:
Pet market
Czech Republic
Introduction pathway
Invasive species
Ornamental animal
AmphISK
a b s t r a c t
The pet trade has grown in recent years and become the most important pathway for the introduction
of non-indigenous species of amphibians and reptiles worldwide. Amphibians traded on the pet market
have been widely overlooked in systematic invasion studies, so their establishment potential and invasion
dynamics remain poorly understood, despite the fact that the impact of invaders from this taxonomic
group on native biota may be considerable. The determination of the most common species of amphibians
traded as pets was based on a survey of the market in the Czech Republic, which is an export hub for
ornamental aquatic animals into the European Union (EU). Subsequently, the establishment potential of
the most common species for EU was determined using a proven risk assessment model. Amphibians that
scored higher than the established species Xenopus laevis were additionally evaluated for their invasion
potential using the Amphibian Invasiveness Screening Kit (AmphISK).
Sixteen species of amphibians in pet market (14 Anura, 2Caudata) have an establishment potential in
the EU. However, none of these species have reached the invasion potential score of already spreading
species X. laevis and Lithobates catesbeianus. The species closest to the threshold value were Lithobates
pipiens and Pelophylax saharicus. Amphibians represent a rather small group within all traded animals
but this fact should not lead us to an underestimation of their potential invasiveness.
© 2016 Elsevier GmbH. All rights reserved.
1. Introduction
Translocation of species and consecutive biological invasions are
regarded as accompanying phenomena of globalization (Ricciardi,
2007). Non-indigenous species are becoming the rule rather than an
exception in many parts of the world (Goodenough, 2010). Despite
the increasing interest of ecologists and conservation biologists in
invasions (Puth & Post, 2005), there is no sign that the introduction
rate of non-indigenous species is slowing (Hulme, Pyšek, Nentwig,
& Vila, 2009).
In an intensively studied group of non-indigenous plant species
most of them established themselves in new regions through unintentional introduction events (Pyšek, Jarošík, & Pergl, 2011). The
situation in relation to vertebrates is the opposite. The reasons
for their intentional introduction are mainly biological control,
source of food, aesthetics and entertainment (Tingley et al., 2010;
Kumschick & Richardson, 2013). This state probably favours successful establishment in a new environment, because intentionally
∗ Corresponding author. Fax: +420 224 382 868.
E-mail address: [email protected] (O. Kopecký).
http://dx.doi.org/10.1016/j.jnc.2016.02.007
1617-1381/© 2016 Elsevier GmbH. All rights reserved.
introduced species are often released in larger numbers and are
afforded greater care in captivity than unintentionally introduced
species (Jeschke & Strayer, 2005; Kraus, 2009).
Among vertebrates, the amphibians have been somewhat overlooked in systematic invasion studies (Henderson, Bomford, &
Cassey, 2011; Poessel, Beard, Callahan, Ferreira, & Stevenson, 2013).
Few highly invasive species, mainly Rhinella marina (Shine, 2010),
Lithobates catesbeianus (Kupferberg, 1997; Pearl, Adamas, Bury, &
McCreary, 2004) and X. laevis (Lillo, Faraone, & Lo Valvo, 2011)
have received attention but establishment potential and invasion
dynamics of other amphibians remain poorly understood (Ernst,
Massemin, & Kowarik, 2011). The impact of amphibian invaders
on native biota may be considerable (Lowe et al., 2000) through
the displacement of indigenous species from their ecological niches
by predation, competition, pathogens introduction or hybridization
(Williamson, 1996; Kraus, 2009).
The project Delivering Alien Invasive Species Inventory for
Europe—DAISIE (2015) reports 36 non-indigenous amphibian
species that briefly appear or have become successfully established
in some parts of Europe. Most of them were translocated within
the continent as in the case of Ichthyosaura alpestris (Lever, 1977),
members of the genus Pelophylax (Holsbeek et al., 2008) and Hyla
O. Kopecký et al. / Journal for Nature Conservation 31 (2016) 22–28
meridionalis (Sillero, 2010). However, successful and now widely
studied are also species originating outside Europe, namely already
spreading X. laevis (Measey et al., 2012) and L. catesbeianus (Ficetola,
Thuiller, & Miaud, 2007). X. laevis is native to the Afrotropical region,
where it lives mainly in stagnant or slow-flowing waters (Tinsley,
Loumont, & Kobel, 1996). The occurrence of X. laevis has been
recorded in several European countries (Measey et al., 2012) and
its negative impact has been reported—e.g. the decline in the number of syntopically living native frogs in Sicily (Lillo et al., 2011). Its
threat to native species is all the more serious as it is a potential
source of the amphibian disease chytridiomycosis caused by the
fungus Batrachochytrium dendrobatidis (Weldon, Du Preez, Hyatt,
Muller, & Speare, 2004). L. catesbeianus was introduced from eastern North America, where it occupies a wide range of wetland
habitats (Adriaens, Devisscher, & Louette, 2013). This species, after
its translocation, negatively affects amphibian communities mainly
through direct predation and competition (Kupferberg, 1997; Pearl
et al., 2004) also in Europe (Thiesmeier, Jäger, & Fritz, 1994). The
presence of infectious B. dendrobatidis on bullfrogs (Garner et al.,
2006), along with other diseases threatening native amphibians,
has been described for European populations, too (Martel et al.,
2012).
The most common introduction pathway for amphibians is the
pet trade, which recently been shown to exceed by almost four
times any other recognizable cause of introduction (Kraus, 2009).
Europe and North America are the main destinations for the export
of ornamental animals (Kraus, 2009; Herrel & van der Meijden,
2014). The most effective management approach is considered to
be identification of the potential danger posed by non-indigenous
species and subsequent prevention of new introductions (Mack
et al., 2000; Thuiller et al., 2005; Keller, Frang, & Lodge, 2008). This
is also true for vertebrates, since the initial stages of introduction
are of crucial importance for successful invasion (Jeschke & Strayer,
2005).
In the present work we focused on assessing the potential risks
of ornamental amphibian species on the territory of EU. This work
responds to a recently published Regulation of the European Parliament and the Council of the EU (No. 1143/2014) on the prevention
and management of the introduction and spread of invasive alien
species, which determines rules for the prevention, minimization
and mitigation of the negative impacts caused by invasive species
and stated that the EU Commission shall adopt a list of invasive
alien species in 2016.
2. Methods
2.1. Identification of ornamental species on the market
The Czech Republic is an export hub of ornamental aquatic
animals for the entire EU (Patoka, Kalous, & Kopecký, 2015). According to laws and regulations in force in the Czech Republic, the
import of live animals and their products are registered by the
Customs Administration of the Czech Republic. Nevertheless, it is
not always possible to identify registered imported amphibians to
species level, which makes these data not entirely suitable for our
study. Therefore to identify species of amphibians that are being
offered in EU countries, we took species listed in Arena, Steedman,
and Warwick (2012) and additionally we surveyed the online price
lists of five leading Czech wholesalers of ornamental animals and
domestic producers of these animals. The survey was performed
during the year 2014. Furthermore, additional discussions were
conducted with wholesalers and producers, who helped us clarify
certain queries or provided supplementary information concerning
the amphibian trade, especially availability on the market.
23
Based on the information obtained, overall 95 species of
amphibians (85 species of the order Anura and 10 species of the
order Caudata) were identified as being on the pet market in the
EU. In accordance with Nentwig, Kühnel, and Bacher (2010) we
restricted our study to species with a native distribution entirely
outside the European continent, mainly from different zoogeographical regions. Two species, Pelophylax esculenta and Pleurodeles
waltl, were excluded, being native to Europe, and 42 species of
anurans were excluded due their rare availability on the market.
On the other hand, we added Pelophylax saharicus to our selection,
due to the fact that it is morphologically similar to other members
of the genus (potential confusion with other species is likely) and
meets our criterion as being of non-EU origin. Another three species
Rhaebo blombergi, Lithobates pipiens and Lithobates clamitans were
added to our list due to their pet trade history, together with their
historical reports of failure establishment in at least one of the EU
countries (Kraus 2009; DAISIE 2015). It follows that 43 species of
frogs and 9 species of newts and salamanders were assessed as
being widely traded.
2.2. Determination of establishment and invasion risks for the EU
We searched the ISI Web of Knowledge for publications about
biology of assessed species, using their scientific names (and if
necessary their older synonyms) as search terms. Furthermore, relevant information provided on websites (www.iucn.org, www.nas.
er.usgs.gov, www.animaldiversity.org, www.amphibiaweb.org) as
well as literature cited therein, were used to compile published
information available on selected species.
As the target region we chose all states of the EU, including the
autonomous islands of Macaronesia (namely the Azores, Madeira
and Canary Islands) in a manner similar to Arnold (2003), while,
due to their geographical remoteness, the overseas departments
and regions of France and Great Britain were not included into our
study as parts of the EU.
We used hierarchically two models for determining the establishment and invasion risk: the Risk Assessment Model (RAM) for
exotic amphibians and reptiles used formerly by the Australian
Bureau of Rural Sciences (Bomford, 2008; Bomford, Kraus, Barry,
& Lawrence, 2009); and, the Amphibian Invasiveness Screening Kit
v 1.19 (AmphISK) developed by CEFAS (Copp et al., 2008).
The species identified as being widely traded were firstly
assessed by RAM, which tested the probability of their establishment, i.e. the formation of a self-sustaining population in a new
environment (Copp et al., 2005), and then all species were evaluated for their invasion potential, i.e. their spread in the new
environment simultaneously producing significant changes in the
composition, structure or processes of the ecosystem (Copp et al.,
2005), in the EU by AmphISK. We decided to use this approach
mainly due to the fact that RAM is a model developed specially
for determination of establishment only, while a major part of
independently scored questions in AmphISK deals with potential
impacts of evaluated species rather than its ability to be introduced
or established.
RAM is based on four parameters: (i) climatic similarity between
the source (native distribution of species) and target regions
(termed climate match risk score); (ii) species’ abilities to establish
populations elsewhere (termed prop.species value); (iii) establishment success of species from the particular family (termed family
random effect); and, (iv) jurisdiction score, which accounts for
expected variability in the establishment success rate due to the
effect of a particular jurisdiction (country, state or province) and
for all evaluated species is constant. The risk score in RAM can
reach values of 0–1, where establishment risk ranks are: low ≤ 0.16;
moderate 0.17–0.39; serious 0.40–0.85; and, extreme ≥ 0.86.
24
O. Kopecký et al. / Journal for Nature Conservation 31 (2016) 22–28
Table 1
Results of a risk assessment model (RAM) and invasion scores from AmphISKcomputed for species of ornamental Anura traded in the EU.
Species
Family
RAM value
RAM risk rank
AmphISK
Leptopelis flavomaculatus
Bombina orientalis
Rhaebo blombergi
Rhinella marina
Ceratophrys ornata
Adelphobates galactonotus
Allobates femoralis
Ameerega trivittatus
Dendrobates auratus
Dendrobates leucomelas
Oophaga pumilio
Phyllobates vittata
Ranitomeya reticulata
Eleutherodactylus martinicensis
Agalychnis callidryas
Hyla cinerea
Hyla versicolor
Litoria caerulea
Litoria chloris
Phyllomedusa hypochondrialis
Pseudacris regilla
Hyperolius fusciventris
Hyperolius tuberilinguis
Kaloula pulchra
Kassina maculata
Kassina senegalensis
Megophrys nasuta
Dyscophus antongilii
Microhyla pulchra
Hymenochirus curtipes
Xenopus laevis
Pyxicephalus adspersus
Hylarana signata
Lithobates catesbeianus
Lithobates clamitans
Lithobates pipiens
Odorrana hosii
Pelophylax saharicus
Ptychadena mascareniensis
Nyctixalus pictus
Polypedates leucomystax
Rhacophorus nigropalmatus
Rhacophorus reinwardtii
Theloderma asperum
Arthroleptidae
Bombinatoridae
Bufonidae
Bufonidae
Ceratophrynidae
Dendrobatidae
Dendrobatidae
Dendrobatidae
Dendrobatidae
Dendrobatidae
Dendrobatidae
Dendrobatidae
Dendrobatidae
Eleutherodactylidae
Hylidae
Hylidae
Hylidae
Hylidae
Hylidae
Hylidae
Hylidae
Hyperoliidae
Hyperoliidae
Hyperoliidae
Hyperoliidae
Hyperoliidae
Megophryidae
Microhylidae
Microhylidae
Pipidae
Pipidae
Pyxicephalidae
Ranidae
Ranidae
Ranidae
Ranidae
Ranidae
Ranidae
Ranidae
Rhacophoridae
Rhacophoridae
Rhacophoridae
Rhacophoridae
Rhacophoridae
0.006–0.100
0.054
0.008
0.109
0.027–0.355
0.006–0.100
0.006–0.100
0.006–0.100
0.006–0.100
0.006–0.100
0.006–0.100
0.006–0.100
0.006–0.100
0.060–0.559
0.021
0.044
0.210
0.183
0.021
0.021
0.321
0.028–0.367
0.029–0.371
0.028–0.367
0.029–0.370
0.086–0.652
0.006–0.100
0.023–0.321
0.025–0.333
0.083
0.365
0.011–0.179
0.321
0.941
0.910
0.819
0.321
0.773
0.597
0.058–0.552
0.037–0.430
0.058–0.552
0.058–0.552
0.058–0.552
low
low
low
low
low–moderate
low
low
low
low
low
low
low
low
low–serious
low
low
moderate
moderate
low
low
moderate
low–moderate
low–moderate
low–moderate
low–moderate
low–serious
low
low–moderate
low–moderate
low
moderate
low–moderate
moderate
extreme
extreme
serious
moderate
serious
serious
low–serious
low–serious
low–serious
low–serious
low–serious
−4
3
−4
15
6
5
5
4
5
2
2
4
2
−1
−2
6
4
9
0
−2
1
3
2
6
0
2
−4
1
6
5
10
6
−2
10
4
6
−5
8
4
−7
5
−4
−4
−6
Note: RAM risk rank based on RAM value refers to establishment potential of evaluated species. AmphISK score, which represent the result of part of questionnaire only,
refers to its invasion potential. The threshold value based on already established and spreading exotic species is 0.365 for RAM and 10 for AmphISK.
Climate match risk scores were computed using the program
Climatch v1.0 (Bureau of Rural Sciences, 2008) with a Euclidean
algorithm and 16 temperature and rainfall variables. Values of
prop.species scores were computed originally for this study using
the Kraus (2009) database. When values for calculating prop.species
or prop.genus were insufficient, we did not compute a prop.family
value (Henderson et al., 2011), but instead used approximation according to phylogenetically related genera (i.e. the closest
branches on an up-to-date phylogenetic tree Pyron & Wiens, 2011).
Family random effects were taken from Bomford (2008). If the value
of family random effect was not listed, we substituted into the formula both theoretical extremes. Then the range of values for risk
score is presented (Bomford, 2008). Before we applied this modification, the model was calibrated on L. catesbeianus and X. laevis for
the EU, and extreme (0.941) and resp. moderate (0.365) risk ranks
of establishment were obtained.
AmphISK is an electronic toolkit, which consists of 49 questions
with three possible answers (Yes/No/Don’t know). There are also
four levels of certainty (from very uncertain to very certain) which
are filled in the application for each particular answer. Some of the
questions deal with biogeographical similarity, including the climate tolerance of evaluated species, and some of the questions
examine undesirable attributes, such as whether the species is
poisonous or if it is a pathogen vector. However, most questions
concern the species’ biological/ecological characteristics that can
facilitate a potential invasion. For evaluating the invasion potential
of ornamental amphibians, we used the sum of the scores from the
questions dealing with undesirable attributes plus those concerning biological/ecological features.
AmphISK questions 37–39 (7.01–7.03 in the report list) are
focused on the passive dispersion potential of species: whether life
stages are likely to be dispersed unintentionally, intentionally by
humans, or as a contaminant of commodities. These characteristics increase the chance that a species can be transported (even
repeatedly) to a new area. In terms of our approach, this chance
is defined by inclusion into our list of the most commonly traded
species. However, these questions can shape the results of AmphISK
by increasing the invasion score. On the other hand, the characteristics assessed by questions 37–39 can play a role also in the
dispersion of species in the new area (“intra-area” transport), thus
facilitating their invasion, as in the case of L. catesbeianus (Ficetola
et al., 2007). For this reason we decided to include these questions
in the total AmphISK invasion score.
The AmphISK invasion score (undesirable attributes
score + biology/ecology score) can reach values from −10
(unpromising invader) to 33 (highly risk invader). Two frogs
O. Kopecký et al. / Journal for Nature Conservation 31 (2016) 22–28
25
Table 2
Results of a risk assessment model (RAM) and invasion scores from AmphISKcomputed for species of ornamental Caudata traded in the EU.
species
family
RAM value
RAM risk rank
AmphISK
Ambystoma maculatum
Ambystoma mexicanum
Ambystoma tigrinum
Cynops orientalis
Cynops pyrrhogaster
Neurergus strauchii
Paramesotriton chinensis
Paramesotriton labiatus
Tylototriton verrucosus
Ambystomatidae
Ambystomatidae
Ambystomatidae
Salamandridae
Salamandridae
Salamandridae
Salamandridae
Salamandridae
Salamandridae
0.625
0.037
0.381
0.090
0.117
0.093
0.084
0.088
0.083
serious
low
moderate
low
low
low
low
low
low
2
0
3
−1
1
−5
−4
−1
1
Note: RAM risk rank based on RAM value refers to establishment potential of evaluated species. AmphISK score, which represent the result of part of questionnaire only,
refers to its invasion potential. The threshold value based on already established and spreading exotic species is 0.365 for RAM and 10 for AmphISK.
L. catesbeianus and X. laevis are already established in Europe, and
they are spontaneously spreading locally (Ficetola et al., 2007;
Faraone, Lillo, Giacalone, & Lo Valvo, 2008). These species of nonindigenous amphibians attained 10 points in invasion potential.
The categorization of evaluated species is not possible, because
we do not use the AmphISK overall score. Due to the character of
questions in AmphISK software, we can argue that the AmphISK
invasion score expresses the species’ potential abilities to spread
in a new environment and to alter the environment either directly
or indirectly. Conclusions concerning the threat (successful establishment and following spread) posed by examined species were
calibrated using the reference species X. laevis and L. catesbeianus.
The relationship of establishment probability and invasion
potential was computed separately for anurans and caudatans as a
correlation of the RAM score with the AmphISK invasion potential
score in Statistica 12 (Statsoft., Inc., 2012).
3. Results
The threshold for establishment was set to the RAM value of
0.365 based on X. laevis as the reference species. Altogether, 16
evaluated species of Anura (Table 1) and two evaluated species of
Caudata (Table 2) were considered as species with an establishment
potential in Europe, i.e. reach RAM value equal or higher than 0.365.
The AmphISK invasion score for threshold species L. catesbeianus
and X. laevis was 10. None of the other evaluated amphibian species
with a RAM establishment value higher than 0.365 attained an
AmphISK score of 10. The highest AmphISK invasion score of 6 and 8
was calculated for L. pipiens and P. saharicus, respectively (Table 1).
We found no correlation between the establishment probability and invasion potential for either Anura (Pearson correlation,
r = 0.203, p = 0.187) or Caudata (Pearson correlation, r = 0.600,
p = 0.116; Fig. 1).
4. Discussion
While introductions of mammals and birds peaked in the 19th
century and those of fish in the 1960s (Jeschke & Strayer, 2005), it
is possible that amphibian introductions have yet to peak. Introductions of amphibians have risen since the second half of the 20th
century, and recently their increment has been significant (Kraus,
2009). We cannot expect the volume of amphibian species traded
as pets to decrease, be it qualitatively (number of exotic species
imported to the EU market) or quantitatively (number of imported
individuals of a particular species; Herrel & van der Meijden, 2014).
Therefore, the aforementioned EU regulation (No. 1143/2014) is
very necessary and of great importance. In terms of its adoption,
legislation of the EU and many of its individual members fails to
anticipate new biological invasions, because their legislation considers exotic species harmless unless their negative impacts are
demonstrated directly in the EU (Holsbeek et al., 2008; Arena et al.,
2012).
Each biological invasion is a complex process that consists
of a sequence of four well-defined stages (García-Berthou, 2007;
Blackburn et al., 2011), and non-indigenous species must successfully pass through all of them to become invasive. The first stage
is “transport” from the place of origin to a new area. The second
phase is characterized by intentional or unintentional release of an
organism by humans into the wild, or by its active or passive escape
from captivity. We further refer to this phase as “introduction”. The
third phase is “establishment” of the organism in the new environment, and the fourth is its unassisted “spread” in the new region
(Williamson, 1996; Kolar & Lodge, 2001; Copp et al., 2005; Tingley
et al., 2010).
The stages “transport” and “introduction” are often poorly documented, with a lack of quantifiable data (Kolar & Lodge, 2001;
Ficetola, Coic et al., 2007; Poessel et al., 2013). The legislative control
of animal imports and related forms of registration vary in different
EU countries (Arena et al., 2012). In the “introduction” phase, there
is a complete lack of estimations concerning escapes from unsecured stock or intentional releases of kept animals into the wild.
If they exist, they can be supposed to be biased, since releasing
imported animals is often illegal, so it is not easy to detect (Drake,
Mercader, Dobson, & Mandrak, 2015).
Our hierarchical approach shows how non-indigenous species
pass through the process of invasion. Similarly to other ornamental
species traded, ornamental amphibians are transported as part of
the pet trade (i.e. pass through the invasive stage “transport”), and
then become part of private stocks, from which they can escape
or can be deliberately released into the wild (e.g. Patoka, Petrtýl,
& Kalous, 2014). This involves the invasive stage “introduction”.
The third stage “establishment” is expressed by scores obtained by
applying one of the most widely used RAM models (Bomford, 2008;
Kumschick & Richardson, 2013). The RAM model used reflects
the most important factor of the invasion process, i.e. climate
match (Thuiller et al., 2005; Ficetola, Coic et al., 2007; Bomford
et al., 2009), but also introduction history and taxonomy (Bomford,
2008). Finally, the invasion potential stage “spread” was evaluated
separately by questionnaires developed on the basis of established
assessment kits for other freshwater animal groups (Copp et al.,
2008). This approach is similar to those used by Fujisaki et al. (2010)
and Masin, Bonardi, Padoa-Schioppa, Bottoni, and Ficetola (2014)
for evaluation of the invasion risk posed by frequently traded reptiles.
The hierarchical process is advantageous because it overcomes
the known problem with risk assessment models—the production of a single unifying factor such as weediness or invasiveness
(Kumschick & Richardson, 2013), which often means confusion or
at least the impossibility of correcting the identification and level
of expression of traits involved in the invasion process (Cassey,
Blackburn, Jones, & Lockwood, 2004). On the other hand, the proce-
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O. Kopecký et al. / Journal for Nature Conservation 31 (2016) 22–28
Fig. 1. Relationship between RAM establishment values and AmphISK invasion scores for evaluated species of ornamental amphibians traded in the EU.
dure described has its limits. Mainly due to the use of a non-specific
jurisdiction score, the RAM establishment value cannot be viewed
as a precise estimation of the probability of establishment, but
rather provides a relative ranking of ornamental amphibians traded
in the EU.
The impact of non-indigenous species in a new environment can
be direct or indirect (Goodenough, 2010). In amphibians we rather
expect direct impacts like predation, competition or disease transmission. This is already true for two species of ornamental frogs that
we have evaluated as being the most dangerous. This concerns L.
pipiens, which tolerates a wide variety of habitats and whose natural range covers different climatic conditions (Fryer & Tunstall,
2001). Its invasion potential is based on its short generation time,
fertility and hosting of diseases (Fryer & Tunstall, 2001; Klemish,
Brooke, Siddons, & Wild, 2012), so its potential negative impact is
caused mainly by competition with native species.
P. saharicus is an ecologically versatile species with a high establishment potential mainly in southern parts of the EU, which are
climatically similar to its native range (Whittaker & Rabie, 2005).
Some individuals reach sexual maturity in the same year they
hatch, but most of them in the second year of their life (Esteban,
Garcia-Paris, Buckley, & Castanet, 1999). They breed and forage
in man-made or various alternate habitats (Whittaker & Rabie,
2005). Their potential spread may be accompanied by hybridization with indigenous species of the genus Pelophylax, as has been
described in the case of non-indigenous congeners from Belgium
(Holsbeek et al., 2008; Holsbeek, Mergeay, Volckaert, & Meester De,
2010). Also probable is direct predation of smaller native species of
amphibians.
The establishment potential of L. pipiens (RAM establishment
value = 0.819) and P. saharicus (RAM establishment value = 0.773)
is high, but their invasion potential (AmphISK = 6 resp. 8) does not
exceed values of the already spreading species X. laevis and L. catesbeianus (AmphISK risk score = 10). Only R. marina scores higher
(AmphISK risk score = 15) than these two species, but a low RAM
establishment value (0.109) shows that this species can have an
impact only in specific regions (particularly Galicia in Spain, northern Portugal, south and east coasts of England, coastal areas of the
Netherlands and Belgium), so its invasiveness potential is at the
most of a local nature.
One may argue that current analyses based on historical data
of climatic patterns may be soon outdated in light of ongoing climate change and global warming (Crowley, 2000). Temperature
is one of crucial patterns in climate match risk score, which is
included in RAM. Increasing temperature in the target area will
facilitate an establishment of ectothermic exotic amphibians. Also
acclimatization (in shorter time interval) or adaptation (in longer
time interval) of non-indigenous species may stimulate the establishment. This was shown for other ectothermic groups of invasive
animals like mussels (Braby & Somero, 2006), true bugs (Coccia,
Calosi, Boyer, Green, & Bilton, 2013), fishes (Iacarella & Ricciardi,
2015), but recently also for already mentioned R. marina (McCann,
Greenlees, Newell, & Shine, 2014). In our scenario, the accessibility of the EU for exotic amphibian species may be underestimated.
In accordance with results achieved by Ricciardi and Cohen (2007),
the RAM establishment value was not correlated with the potential
negative impact of species, i.e. with the AmphISK invasion score in
our case. This finding justifies the hierarchical use of two models.
The strength of correlation is higher for Caudata than Anura, but
differences in sample size can play a role in this relationship.
Defining the RAM establishment value is also based on the realized niche of the species within their native range (Kearney, 2006).
However, interactions in the non-indigenous range can modify
the dimensions of the realized niche (Broennimann et al., 2007).
In this context, the hypothesis of biotic acceptance/resistance
is widely discussed (Stohlgren, Jarnevich, Chong, & Evangelista,
2006). Poessel et al. (2013) found support for the biotic acceptance hypothesis for amphibians in Europe, which suggest that
amphibian communities in Europe are not saturated. Therefore
future monitoring should be focused on climatically suitable places:
islands and coastal areas of the Mediterranean and lowlands in
northern Greece, Bulgaria, Romania, Slovakia and the Sava valley
of Croatia, regardless of the diversity of indigenous communities
living there.
When the attention is put on recipient amphibian communities,
also the factor of relatedness of indigenous and non-indigenous
species can play a role in establishment of invaders (Strauss, Webb,
& Salamin, 2006). For amphibians it was calculated that establishment success increases when species from the same genus
were present at the locations of introduction (Tingley et al., 2010).
O. Kopecký et al. / Journal for Nature Conservation 31 (2016) 22–28
Unfortunately, this fact is not taken into account in the RAM establishment model, where “biotic” values of prop.species and family
random effect remain constant regardless of the target area evaluated (Bomford, 2008). Therefore we have to point out the possibility
that RAM establishment values for the species Bombina orientalis,
Hyla cinerea, Hyla versicolor and P. saharicus can be higher due to
the presence of congeners in recipient amphibian communities.
Although the crucial component of invasion success is propagule pressure (Kolar & Lodge, 2001; Ficetola, Coic et al., 2007; Wilgen
& Richardson, 2012), it is usually only estimated from known correlations. High availability of non-indigenous species on the local
market leads to higher sales and consequently to a higher rate of
escapes and releases, as documented in the case of reptiles traded in
Florida (Fujisaki et al., 2010) or Trachemys scripta in Europe (Cadi &
Joly, 2004). Although it is less likely, it cannot be fully excluded that
species rarely available on the market (in our case 42 not evaluated
species of traded exotic amphibians), may established themselves
in the wild within the EU despite their low propagule pressure.
The import of species for the pet trade is concentrated mainly
in densely populated (Copp, Vilizzi, & Gozlan, 2010) and wealthy
(Pyšek et al., 2010) areas, where the highest propagule pressure
of non-indigenous species can be expected. In comparison with
current invasive species in the EU (X. laevis, L. catesbeianus), the
ornamental amphibians assessed are probably less dangerous in
regards to propagule pressure. Additionally, already spreading
species probably exert long-term and higher propagule pressure.
The worldwide spread of X. laevis started in the first half of the
20th century, after the development of a pregnancy test using frog
as a test animal, as well as its use as a model in developmental biology (Measey et al., 2012). L. catesbeianus was imported to Europe
mainly for food production already in the 19th century, and the
most important pathway for introduced populations were escapes
from frog farms (Adriaens et al., 2013). From this point of view,
P. saharicus has a specific position among the species evaluated.
As another non-protected sibling species of the genus Pelophylax it
may be imported to the EU to be kept in ornamental garden ponds
(Holsbeek et al., 2008, 2010), from where it can easily escape into
the wild.
5. Conclusions
It is expected that exotic amphibians may affect native amphibian species, primarily by predation, competition and disease
transmission and thereby contribute to the decline of these globally
threatened animals (Stuart et al., 2004). Our analyses revealed that
at least 96 species of exotic amphibians are sold on the pet market
in the Czech Republic, and redistributed to the entire EU. Sixteen
of them show an establishment potential in the EU, while L. pipiens
and P. saharicus have additionally an invasive potential. These findings result in recommendations for trade restrictions/regulations
for at least these two species. Although the amphibians represent a
rather small group within all traded animals, it should not lead us
to an underestimation of their potential invasiveness.
Acknowledgement
We thank Mary Bomford for her dedication to the question of
risk assessment. This study was supported by CIGA Project No.
20152007 of the Czech University of Life Sciences Prague. The
English was corrected by a Frederick Rooks (English Language Services).
27
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