Assessing the risk of freshwater fish introductions into
the Iberian Peninsula
M I G U E L C L AV E R O * , †
*Doñana Biological Station, Department of Conservation Biology, CSIC, Sevilla, Spain
†
Grup d’Ecologia del Paisatge, Àrea de Biodiversitat, Centre Tecnològic Forestal de Catalunya, Carretera vella de Sant
Llorenç de Morunys, Solsona, Spain
SUMMARY
1. Preventing the introduction of species likely to become invaders is the best management
option to deal with biological invasions. A data set consisting of native, introduced and
species not currently present in Iberian Peninsula (n = 167 species) was used to identify
freshwater fish species that are likely to be introduced and become successful invaders in
the near future.
2. Principal component analysis (PCA) of species traits was used to determine species
likely to be introduced, assuming that the traits of species introduced in the future will
resemble those of previously introduced species. The likelihood of introduction was
calculated as the proportion of neighbour species (in the space defined by the PCA) that
have been introduced to the Iberian Peninsula and, together with metrics related to
different stages of invasion, was used to construct a region-specific risk index (Iberian risk
index).
3. Introduced species had higher index values compared with native species or species
currently absent from the region. The Iberian risk index was positively related to the
results of an independent risk analysis for freshwater fish as well as to the geographical
spread of species previously introduced to the Iberian Peninsula.
4. Iberian risk index values were used to establish a cut-off value for estimating the
probability of a successful invasion. This threshold value was used to construct a list of 20
species to be included in a ‘watch list’ to prevent freshwater fish invasions in the Iberian
Peninsula.
Keywords: environmental management, invasive species, Mediterranean streams, risk analysis, watch
lists
Introduction
The introduction of non-native species into new
environments and their spread over natural areas
pose important threats for the conservation of biodiversity (Mack et al., 2000; Clavero & Garcı́a-Berthou,
2005). Despite growing concern of the negative
impacts of many non-native species on biodiversity,
Correspondence: Miguel Clavero, Doñ ana Biological Station,
Department of Conservation Biology, CSIC, Americo Vespucio
s⁄n, 41092 Sevilla, Spain. E-mail: miguelclavero@ebd.csic.es
human activity continues to facilitate the transport of
species across biogeographical barriers. Some of these
non-native species cannot establish self-sustaining
populations in their new habitats and eventually
disappear, whilst others thrive, become abundant and
expand their ranges, subsequently acquiring the
status of invasive species (Lockwood, Hoopes &
Marchetti, 2007). Recent effort has focussed on trying
to identify the characteristics of invasive species to
better understand why some species are more successful than others (Kolar & Lodge, 2001). Indeed,
species profiling may be useful to identify species that
are likely to become invaders, potentially providing a
valuable tool to prevent future invasions or mitigate
their effects. The most commonly applied output of
invasive species profiling is risk analysis, which aims
to quantify the likelihood that a species will become
established and⁄or will result in environmental impacts (Andersen et al., 2004; Baker et al., 2008).
Since the eradication or control of established
introduced species is often costly, difficult and generally impracticable management actions (e.g. Mack
et al., 2000), preventing an introduction is considered
as the best alternative to avoid new invasions (Keller,
Lodge & Finnoff, 2007; Hulme et al., 2008). However,
since it is not possible to stop international movements of all live organisms or to forbid the tenancy of
every non-native species (e.g. Keller & Lodge, 2007),
legislators dealing with biological invasions need to
decide which non-native species should be subjected
to regulation. Two alternative approaches are often
considered in developing regulatory procedures. Following a precautionary principle (‘guilty until proven
innocent’), the first option is to require the assessment
of the invasiveness of any imported species. Species
classified as having low invasive potential are
included on a ‘white list’ (e.g. Wittenberg & Cock,
2001). The second approach is to construct ‘watch
lists’ or ‘black lists’ that include non-native species
that should not be imported or maintained in a given
territory. Black listing is commonly used to denote
invasive species that have become established in a
given territory and are subjected to regulation, while
species not yet present but considered as likely future
invaders are included on watch lists (EEA, 2010).
However, management authorities often have difficulty in determining which species should be
included on watch lists. For example, information
concerning the characteristics of a potential invader
and potential donor regions or species pools is often
lacking. Moreover, since many of these factors may be
region specific, decisions adopted in one country or
territory may not always be applicable to other areas
(e.g. Moyle & Marchetti, 2006).
Freshwater ecosystems are especially sensitive to
biological invasions, and not surprisingly, some of the
most striking examples of the impacts that invasive
species have on ecosystem structure and function
come from aquatic environments (e.g. Darwall et al.,
2008). The Mediterranean Basin is a global hot spot for
freshwater fish invasions (Leprieur et al., 2008), with
many endemics threatened by invasive species (Clavero et al., 2010). For example, the main river basins of
the Iberian Peninsula currently have more exotic than
native fish species (Clavero & Garcı́a-Berthou, 2006).
Although the mechanisms involved in the interactions
between native and exotic species are often unclear
(e.g. Leunda, 2010), it has been shown that invasive
fish species are an important and probably the main
threat for Iberian native icthyofauna (Maceda-Veiga
et al., 2010; Hermoso et al., 2011). Moreover, new fish
species are being introduced to the Iberian Peninsula
(e.g. Franch et al., 2008; Gante et al., 2008), while
previously established species are expanding their
ranges (e.g. Vinyoles et al., 2007; Ribeiro et al., 2009a).
In this context, the identification of fish species that
could be introduced in the near future is important to
prevent further invasions.
Here, I apply a region-specific procedure to identify
likely future introductions into the Iberian Peninsula
and the risks associated with new invasions using
freshwater fish as case study. When trying to identify
successful invaders, a series of sequential stages
(transport, introduction, establishment, spread and
impact) and traits that may influence the success of
species need to be considered (Marchetti, Moyle &
Levine, 2004; Ribeiro et al., 2008). As a first step, I used
a multivariate approach to quantify the likelihood of
introduction of freshwater fish that are not yet present
in the Iberian Peninsula. I compared the traits of fish
species that are native to or have been introduced into
the Iberian Peninsula with species that could potentially be introduced. In a second step, I complemented
the likelihood of introduction with metrics related to
the different stages of the invasion process to generate
a region-specific risk index for freshwater fish invasions. My main aims were to provide an objective
account of plausible future fish introductions and
subsequent invasions and to provide a useful tool for
biodiversity managers both in the Iberian Peninsula
and elsewhere.
Methods
Species included in the analyses
The pool of fish species considered in the analyses
was limited to (i) species that are present, either as
native or as introduced, in the Iberian Peninsula
and⁄or neighbouring European countries (France,
Italy, Switzerland, Germany, Belgium, the Netherlands, England and Wales) or (ii) species that have
been introduced in Europe, independently of whether
they are known to have established self-sustained
wild populations. North African species were excluded from the analysis because of the paucity of
ecological information (e.g. Smith & Darwall, 2006)
and because almost all fish introductions in the
Iberian Peninsula come from Europe, and none thus
far has been documented from northern Africa (Garcı́a-Berthou et al., 2005). The analysis was limited to
bony fish, thus excluding lampreys. Kottelat & Freyhof (2007) were used to select the pool of species
analysed, supplemented with species used by Copp
et al. (2009) to calibrate a risk analysis for freshwater
fish [the fish invasiveness scoring kit, (FISK)] and with
other fish species that have been introduced to the
Iberian Peninsula (Gante et al., 2008; Ribeiro et al.,
2008). I excluded some range of restricted salmonid
species that are endemic to single or small groups of
lakes (mainly in the genera Coregonus, Salvelinus and
Salmo). The final list included 227 freshwater fish
species and followed the taxonomic nomenclature of
Fishbase (Froese & Pauly, 2010).
Likelihood of introduction
Twelve variables characterising biogeographical features and human uses were used to quantify the
likelihood of introduction into the Iberian Peninsula
(Table 1). Unless stated otherwise, variables were
obtained from Fishbase, a database including information on about 32 000 fish species (Froese & Pauly,
2010). The final data set, excluding species for which
information was incomplete, comprised 167 species
(Table S1).
I collected data on the number of countries or
territories (in Fishbase) where each species is native,
excluding those in which the presence of the species
was coded as ‘questionable’ or ‘misidentification’. The
distribution of each species was further characterised
by the average latitude of their native range (i.e. the
mean between maximum and minimum latitudes)
and the range of latitudes occupied (i.e. the difference
between maximum and minimum latitudes). When
distributions occurred on both sides of the equator,
the latitudinal range was set to the maximum latitude
occupied. The introduced range of each species was
described by the number of countries or territories
where the species had been introduced, independent
of whether introductions resulted in established populations.
I included popularity in the analyses assuming that
the most popular species would be more likely to be
introduced into the region. Popularity for each species
was evaluated using Google web browser. I introduced the Latin names in quotes and recorded the
number of results of the search. The search procedure
Table 1 Variables used to describe the characteristics of fish species used in the calibration of the Iberian risk index. Data transformations (Transf.) are indicated, with a dash denoting no transformation. For continuous variables, numbers in brackets indicate
the range of values (minimum and maximum). The inclusion of each variable in the principal component analysis (PCA, see Fig. 1)
is also stated
Total length
Native countries
Average latitude
Latitude range
Introduced countries
Popularity
Iberian popularity
Game fish
Aquaculture
Fisheries
Aquarium
Bait
Status in France
Habitat breadth
Climatic mismatch
Parental care
Pest
Code
Values (min, max)
Units
Transf.
PCA
SIZE
NATI
avLAT
raLAT
INTR
POPU
POPIBE
GAME
AQRE
FISH
AQUM
BAIT
Continuous (4.5, 800)
Continuous (1, 55)
Continuous (0.5, 60.5)
Continuous (1, 67)
Continuous (0, 121)
Continuous (406, 543000)
Continuous ()1.9, 1.5)
0, 1, 2
0, 1, 2
0, 1, 2
0, 1, 2
0, 1, 2
Absent, nativeand introduced
1–5
Continuous (0, 39.5)
Yes, no
Yes, no
cm
Count
Degrees
Degrees
Count
Count
Count (residual)
None
None
None
None
None
None
Count
Degrees
None
None
log10X
X
X2
–
X
log10X
–
–
–
–
–
–
–
–
X
–
–
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
No
No
No
No
No
was then restricted to Spanish and Portuguese pages
to obtain an Iberian index of popularity. Residuals of
the number of results of the Iberian search regressed
against the number of results of the unrestricted
search (log10-transformed in both cases; F1,165 = 78.1;
P < 0.001; R2 = 0.32) were used as an indicator of the
relative popularity of each species in the Iberian
Peninsula. Human uses of each species were characterised by coding game fish, aquaculture, fisheries,
aquarium and bait from 0 to 2: 0 = ‘no use’,
1 = ‘minor use’ or ‘occasional use’ and 2 = ‘otherwise’
(according to Fishbase). Since introduced fish species
have larger body size than expected by chance alone
(Blanchet et al., 2010), I also included maximum
length (in cm) of each species in the analysis of the
likelihood of introduction.
Principal component analysis (PCA) with varimax
normalised rotation (McGarigal, Cushman & Sttaford,
2000) was used to summarise the variation in variables related to the likelihood of introduction. Only
the first three axes were used since preliminary
analyses showed that these axes explained most of
the total variance. Position in the three-dimensional
space defined by the three axes (PC1, PC2 and PC3)
was used to indicate fishes likely to be introduced in
the Iberian Peninsula. Differences in the average
position of absent, introduced and native Iberian
species along the three axes were analysed using oneway A N O V A s. A dissimilarity square matrix from the
scores of each species along the three principal
components (PCs) using Euclidean distances was
calculated and used to estimate the percentage of
introduced neighbours for each species (counts of
neighbours within a given radius). The radius was set
as the average distance of the 25th nearest neighbour
for the 167 species included in the PCA. In 18 cases,
the number of neighbours within the fixed radius was
<10; here, I used the 10 nearest species to calculate the
percentage of introduced neighbours. This index,
which ranged from 0 to 69%, was used to estimate
the likelihood of introduction, under the assumption
that the characteristics of fish species introduced in
the future will resemble those of current introduced
species.
Risk index for the Iberian Peninsula
Together with the likelihood of introduction, additional metrics related to different stages of the invasion
process were used to produce the Iberian risk index
for freshwater fish. First, the probability of introduction was complemented by the status of each species
in France (either absent, native or introduced). France
is the main donor region of introduced fish to the
Iberian Peninsula (Garcı́a-Berthou et al., 2005), and
most species introduced to Iberia have been introduced earlier to France (Clavero & Garcı́a-Berthou,
2006). Therefore, I assumed that the probability of
introduction of a given species to the Iberian Peninsula
was greater if currently found in France and greater
still if an introduced rather than a native species.
Three variables related to the probability of establishment of introduced species were included in the
index. (i) A measure of habitat breadth was calculated
using the habitat preferences (streams⁄creeks, rivers,
lentic environments, brackish areas and sea) reported
in fishbase. Habitat breadth was calculated as the sum
of the citations of the use of these habitats by each
species (range 1–5), with larger values indicating
wider niche breadth. Species with wider niche
breadths were assumed to have higher probabilities
of establishing in the wild after introduction. (ii) The
mismatch between the native range of each species
and the climatic conditions of the Iberian Peninsula
was calculated as the difference between average
latitude and the mean of the average latitudes of
Iberian endemic species (n = 24). Large values denote
that the centre of the distribution of a potential
invasive species differs from climatic conditions of
the Iberian Peninsula. Species that have evolved
under climatic conditions similar to the Iberian Peninsula were assumed to have a greater probability of
successful establishment if introduced (Bomford,
Barry & Lawrence, 2010). (iii) Since previous studies
(e.g. Marchetti et al., 2004) have shown that parental
care may be advantageous in the establishment stage
of the invasion process, egg or brood guarding
(including nest and mouth guarders as well as live
bearers, but not egg-hiders), coded as a binary
variable, was used.
Spread and impact stages were included by the
characterisation of species as a ‘potential pests’.
According to Fishbase, a species is considered a
potential pest when, once it has been introduced, it
has the potential to spread quickly and threaten native
species. This classification has been previously used to
calibrate other risk indices developed for freshwater
fish (e.g. Copp et al., 2009).
In summary, the Iberian risk index included metrics
related to the sequential stages of the invasion
process: introduction (likelihood of introduction and
status in France), establishment (habitat breadth,
climatic mismatch and parental care) and spread⁄impact (classification as ‘potential pest’). The scores
given to the three categories are shown in Table 2. The
three variables related to the establishment stage were
summarised in a single metric by calculating the
average (integer) of the scores of the three variables.
Scores assigned to the likelihood of introduction
ranged from 0 to 10, whereas scores of the other
variables ranged from 0 to 5 to double the weight
given to introduction in the final index. The final
Iberian risk index ranged from 0 (minimal risk of
invasion) to 25 (high risk).
Differences in the risk index
between absent,
introduced and native Iberian species were analysed
by one-way A N O V A s, testing the hypothesis that, on
average, risk values should be higher for previously
introduced species than for native ones or the pool of
species that have not yet been introduced. I also
compared the values of the risk index of successful
and failed introductions, the latter being those that
have not produced self-sustained populations as well
as recent introductions with unknown fate. The
Iberian risk index was also related to two independent
indexes related to invasive fish species. First, I collated
information on the invasive potential of 63 species
included in my data set from a risk analysis developed for freshwater fish (FISK; Copp et al., 2009),
testing the hypothesis that FISK values are positively
related to the risk index calculated for the Iberian
Peninsula. Second, I related the risk index to the
spread of each fish species introduced to the Iberian
Peninsula to test whether introduced species with
high Iberian risk values have effectively expanded
across the Iberian Peninsula. As a measure of spread, I
recorded the number of basin groups occupied by 20
species introduced in the Iberian Peninsula (Ribeiro
et al., 2008), updated using recent publications (e.g.
Benejam et al., 2007; Vinyoles et al., 2007; Franch et al.,
2008; Hermoso, Blanco-Garrido & Prenda, 2008;
Ribeiro et al., 2009a).
Results
The first three PCs explained 62% of the variance of
the original 12 variables (Fig. 1). The first axis (PC1)
was positively related to the size of fish and their use
as game fish, in aquaculture and in fisheries, as well as
to their popularity and the number of countries in
which they have been introduced. The second axis
(PC2) was mainly related to the characteristics of
native ranges, with positive values interpreted as
indicating species that are native to many countries,
have wide latitudinal ranges, tend to have northern
distributions and are used as bait. The third axis (PC3)
was positively related to popular, aquarium fish
species that have been introduced to many countries.
Species introduced to the Iberian Peninsula had
significantly higher scores along the three PCs than
native species (one-way A N O V A ; Tukey’s HSD test for
unequal sample sizes P £ 0.005, in all cases), with
absent species scoring at intermediate positions. Redbelly [Tilapia zillii (Gervais, 1848)] and Nile [Oreochromis niloticus (Linnaeus, 1758)] tilapias had the highest
likelihood of introduction scores (69.2 and 62.5% of
introduced neighbours, respectively). Other species
with high likelihood of introduction values (>50% of
Table 2 Variable scores classified according to stages of the invasion process (introduction, establishment, spread–impact) used in the
calibration of the Iberian risk index. The scores of % introduced neighbours varied between 0 and 10 (indicated in parenthesis),
while all other scores varied between 0 and 5. A dash indicates scores that were not available. The scores of the three variables
related to establishment were averaged to obtain a single metric rounded to the nearest integer
Introduction
Establishment
Spread–impact
Score
% Introduced neighbours
Status in France
Habitat breadth
Climatic match
Parental care
Potential pest
5
4
3
2
1
0
‡50
30–<50
20–<30
10–<20
>0–<10
0
Introduced
–
Native
–
–
Absent
5
4
3
2
1
–
0–<1
1–<4
4–<9
9–<16
16–<25
‡25
Yes
–
–
–
–
No
Yes
–
–
–
–
No
(10)
(8)
(6)
(4)
(2)
Fig. 1 Principal component analysis (PCA) of species traits
describing the characteristics of 167 freshwater fish species. Left
panels show the loadings of each original variable for the first
three principal components (PCs). Variable codes are given in
Table 1. Right panels show the position of each species in the
space defined by the first three PCs. Filled circles (•) denote
native fish species, empty circles (s) denote introduced species,
and crosses (+) denote species that are absent from the Iberian
Peninsula.
introduced neighbours) were the blue and Mozambique tilapias [Oreochromis aureus (Steindachner, 1864)
and O. mossambicus (Peters, 1852), respectively], common carp (Cyprinus carpio Linnaeus, 1758), Crucian
carp [Carassius carassius (Linnaeus, 1758)], bighead
carp [Hypophthalmichthys nobilis (Richardson, 1845)],
rainbow trout [Oncorhynchus mykiss (Walbaum, 1792)],
the channel catfish [Ictalurus punctatus (Rafinesque,
1818)] and largemouth bass [Micropetrus salmoides
(Lacepè de, 1802)]. Some species that are native to
the Iberian Peninsula, such as European eel [Anguilla
anguilla (Linnaeus, 1758)] and brown trout (Salmo
trutta Linnaeus, 1758), also had large percentages of
introduced neighbours (50 and 43%, respectively). By
contrast, almost half of the species that did not have
any introduced neighbour (21 of 48) were Iberian
endemics. Among the 27 absent species without
introduced neighbours, 15 were European cyprinids,
some of which were range-restricted species [e.g.
Alburnus albidus (Costa, 1838) or Rutilus rubilio (Bonaparte, 1837)]. None of the species introduced to the
Iberian Peninsula lacked introduced neighbours (see
complete results in Table S1). Interestingly, species
classified as potential pests by Fishbase tended to
have a large proportion of introduced neighbours
(Fig. 2).
Iberian risk index values were clearly influenced by
the status of species in the Iberian Peninsula (one-way
A N O V A P < 0.001; Fig. 3), higher for introduced species than for native ones, with absent species having
intermediate values (HSD test P £ 0.003 in the three
pairwise comparisons). Introduced species that had
successfully established populations had higher Iberian risk index values than unsuccessful introductions
or those with uncertain success (Fig. 3; one-way
A N O V A P = 0.001). The lower limit of the 33.3%
quartile of the Iberian risk index for previous introduced species (14) was used as the cut-off to define
absent species likely to be introduced and become
invasive (Fig. 3). Introduced species with Iberian risk
values <14 tended to fail at establishing wild populations (7 of 10), while failed introductions were rare
for species scoring ‡14 (3 of 23). This threshold
(Iberian risk index score ‡14) resulted in a list of 20
species currently absent, constituting a proposed
watch list for invasive freshwater fish for the Iberian
Peninsula (Table 3).
Fig. 2 Proportion of potential pest and non-pest (harmless)
species classified according to Fishbase (Froese & Pauly, 2010),
for the six categories of the likelihood of introduction variable.
The six categories are given in Table 2. The numbers in brackets
denote the number of species included in each level of likelihood
of introduction.
Identifying future fish introductions
(a)
(b)
(c)
Fig. 3 Iberian risk index values for freshwater fish species that
are absent (a), introduced (b) or native (c) to the Iberian Peninsula. The broken lines mark the threshold used to designate
likely future invasions (Iberian risk index ‡14; see Table 3). In
the introduced species panel, grey bars denote species that have
not been able to establish self-sustained wild populations or
those of uncertain success after introduction, while black bars
denote established introduced species.
The Iberian risk index was positively related to
FISK scores, derived from a risk analysis developed
independently from my data set, as well as to the
spread of previous introduced species in the Iberian
Peninsula (Fig. 4).
Discussion
Developments of risk assessment protocols for invasive species have followed two alternative approaches. One
approach has
been
to use
questionnaires that are summarised in a final risk
score. Proposed by the Australian weed risk assessment programme (Pheloung, Williams & Halloy,
2151
1999), the approach has been adapted to different
taxa, including freshwater fish (e.g. Copp et al., 2009).
The second approach uses statistical inference to
identify features that characterise successful invaders
and then use these variables to predict the probability
of future invaders (e.g. Kolar & Lodge, 2002; VallIlosera & Sol, 2009). Here, I used a multivariate
statistical technique to describe the characteristics of
introduced species to identify plausible future introductions. These results were then transformed into a
scoring system to assess the likelihood of introduction, which was further complemented other with
scores related to different stages of the invasion
process and based on the findings from previous
studies.
The main assumption of my analysis was that
species that are most likely to be introduced into the
Iberian Peninsula are those that have attributes
similar to species that have previously been introduced. My aim was not to describe which features
characterise successful invaders, but to identify species with attributes that are similar to those that have
been introduced. However, patterns revealed by PCA
are generally in agreement with those from previous
studies. For example, the most widely introduced
species in the Iberian Peninsula and elsewhere tend to
be large fish favoured for food and⁄or as game fish
(e.g. Moyle & Marchetti, 2006; Blanchet et al., 2010) or
aquarium fish (Courtenay, 1999; Padilla & Williams,
2004). It must be noted that the main assumption of
the analysis could be unrealistic if the characteristics
of newly introduced fish species differ markedly from
those of fish introduced in the past. However, this
does not seem to be the case, at least regarding the
patterns of the most recent introductions. Of the five
fish species introduced to the Iberian Peninsula after
2000, four [Abramis brama (Linnaeus, 1758), Misgurnus
anguillicaudatus (Cantor, 1842), Pseudorasbora parva
(Temminck & Schlegel, 1846) and Poecilia reticulate
Peters, 1859] had an Iberian risk index score ‡14 and
therefore would have been included on the watch list
shown in Table 3. The fifth species [Barbonymus
schwanenfeldii (Bleeker, 1853)] had an Iberian risk
score of 11, but of the five species, it is the only one
that is not known to have established self-sustained
wild populations. Moreover, as discussed later, the
watch list could include fish species that have been
previously introduced to the Iberian Peninsula,
although not yet reported in the literature.
2152 M. Clavero
Table 3 List of 20 freshwater fish species most likely to become new invaders in the Iberian Peninsula
Order
Family
Species
Risk index
Cyprinodontiformes
Perciformes
Perciformes
Cypriniformes
Cypriniformes
Siluriformes
Perciformes
Cypriniformes
Cypriniformes
Perciformes
Perciformes
Cyprinodontiformes
Cypriniformes
Perciformes
Cypriniformes
Perciformes
Cyprinodontiformes
Salmoniformes
Cypriniformes
Esociformes
Poeciliidae
Cichlidae
Cichlidae
Cyprinidae
Cyprinidae
Ictaluridae
Centrarchidae
Cyprinidae
Cyprinidae
Cichlidae
Cichlidae
Poeciliidae
Cyprinidae
Percidae
Cyprinidae
Gobiidae
Poeciliidae
Salmonidae
Cyprinidae
Umbridae
Gambusia affinis
Oreochromis niloticus
Oreochromis mossambicus
Carassius carassius
Hypophthalmichthys nobilis
Ameiurus nebulosus
Micropterus dolomieu (Lacepè de, 1802)
Hypophthalmichthys molitrix (Valenciennes, 1844)
Pimephales promelas (Rafinesque, 1820)
Tilapia zillii
Oreochromis aureus
Xiphophorus helleri (Heckel, 1848)
Phoxinus phoxinus
Gymnocephalus cernua
Leuciscus leuciscus (Linnaeus, 1758)
Neogobius melanostomus (Pallas, 1814)
Xiphophorus maculates (Gü nther, 1866)
Thymallus thymallus (Linnaeus, 1758)
Mylopharyngodon piceus (Richardson, 1846)
Umbra pygmaea (DeKay, 1842)
24
23
23
22
22
21
20
19
19
18
18
18
18
17
17
17
16
15
14
14
The Iberian risk index was found to be a good
predictor of the probability that introduced fish
species become invasive in the Iberian Peninsula. Of
the 19 species with Iberian risk index values ‡20, 12
(63%) have already been introduced to the Iberian
Peninsula and all but one [the grass carp, Ctenopharyngodon idella (Valenciennes, 1844)] are known to have
established populations (see Table S1). By contrast, of
the 58 species with scores £5, not a single species has
been introduced to the Iberian Peninsula. Thus, the
index predicted a high risk potential for many of the
invasive fish species already present in the Iberian
Peninsula (Fig. 3). Moreover, introduced species that
are widely distributed across the Iberian Peninsula
tend to score higher than those with restricted
distributions, indicating that the index is a good
predictor of the ecological success of a species once it
is introduced. Notable exceptions are species that
have been introduced recently, such as topmouth
gudgeon (P. parva) (Caiola & de Sostoa, 2002), or
species that are currently expanding their ranges,
such as channel catfish (I. punctatus) (Hermoso et al.,
2008).
The 20 species listed as likely future invaders
include some that could already be present in the
Iberian Peninsula. For example, Kottelat & Freyhof
(2007) included the Iberian Peninsula within the
introduced range of C. carassius, highlighting the need
to clarify the specific status of some Iberian Carassius
populations traditionally assigned to C. auratus
(Linnaeus, 1758) (Doadrio, 2002). The western mosquitofish [Gambusia affinis (Baird & Girard, 1853)] has
often been confounded with the eastern mosquitofish
(Gambusia holbrooki Girard, 1859) across their global
introduced ranges. Only recent work has clearly
shown that G. affinis is not present in the Iberian
Peninsula and that all Gambusia populations in the
Mediterranean correspond to G. holbrooki (Vidal et al.,
2010). Similar uncertainties in taxonomy have occurred with black and brown bullheads [Ameiurus
melas (Rafinesque, 1820) and
Ameiurus nebulosus
(Lesueur, 1819); see Kottelat & Freyhof, 2007]; the
former being an invasive species in the Iberian
Peninsula and the latter a likely future invader. The
minnow [Phoxinus phoxinus (Linnaeus, 1758)] was
considered an invasive species in large parts of the
Iberian Peninsula (e.g. Doadrio, 2002), until recent
findings revealed that populations corresponded to
repeated translocations of a congeneric endemic
species (Phoxinus bigerri Kottelat, 2007) native to
north-eastern Spain (Kottelat
& Freyhof, 2007).
Although it may seem unlikely that G. affinis, A. nebulosus or P. phoxinus will be introduced to the Iberian
Peninsula, owing
to the presence of introduced
congeners, the risk index correctly identified their
high invasive potential. Finally, two Xiphophorus
Identifying future fish introductions
(a)
(b)
Fig. 4 Relationships between the Iberian risk index and (a)
average fish invasiveness scoring kit index scores (Copp et al.,
2009) (upper panel) and (b) the number of groups of basins
occupied in the Iberian Peninsula (Ribeiro et al., 2008) updated
with more recent information (lower panel). The positions of
Ictalurus punctatus (Rafinesque, 1818) (Ipu) and Pseudorasbora
parva (Temminck & Schlegel, 1846) (Ppa) are marked in the
lower panel and further commented in the discussion section.
The coefficient of determination (R2) is shown for both relationships.
species were identified as potential future invaders,
coinciding with the recent observation of a yet
unidentified, probably established Xiphophorus population in north-eastern Spain (N. Franch, pers.
comm.).
Identification of species that are currently invasive
or likely to become invasive in the near future is a
requisite tool for management focused on the prevention of new invasions (Hulme et al., 2009). Recently,
the Spanish Law for Natural Heritage and Biodiversity (42⁄2007 December 13th; http://www.boe.es/
aeboe/consultas/bases_datos/doc.php?id=BOE-A-200721490) mandated the development of a list of invasive
species, called the Spanish catalogue of invasive alien
2153
species (SCIAS), to be developed. The law prohibits
release into the environment of species included in the
SCIAS as well as their possession and commercialisation. Results from the present study provide an
objective basis for constructing a watch list for
freshwater fish to be included in the SCIAS. This
watch list is important not only for Spain, but also for
Portugal, since the main pathway of fish introductions
into the Iberian Peninsula is via France, with
subsequent expansions into Portugal (Clavero &
Garcı́a-Berthou, 2006; Ribeiro, Collares-Pereira & Moyle, 2009b). Here, I propose a watch list for freshwater
fish based on the scores of current introduced species,
although the list could be shortened or extended by
changing the risk threshold for the inclusion of
species. This watch list should be dynamic and
adapted to the potential arrival of new species not
considered here (e.g. through the establishment of
new invasion pathways); the analytical procedure
could be repeated to include new species or the
analysis expanded to include a larger pool of species.
Since the risk index proposed here has been
specifically designed for the Iberian Peninsula, it
should not be directly transposed to other territories.
For example, some species that have a large likelihood
of becoming invasive in the Iberian Peninsula are
native to other European countries [e.g. C. carassius or
Gymnocephalus cernua (Linnaeus, 1758)]. Indeed, the
dual status (native and invasive) of many species
within Europe hinders the development of a single
European black list of invasive species (Hulme et al.,
2009). However, the regional approach used here to
identify future invaders, based on the characteristics
of current invaders, can be easily applied to other
regions. Ideally, the assessments of risk of invasion
should consider biogeographically coherent regions
(e.g. river basins or relatively isolated territories), even
though the management outputs are likely to be
dependent on political borders.
Acknowledgments
This work greatly benefited from comments by Nú ria
Roura-Pascual, Virgilio Hermoso, the handling editor
and two anonymous referees. MC held a Ramon y
Cajal contract funded by the Spanish Ministry of
Education and Science (MEC) and received support
from the Consolider Montes CSD2008-00040 project,
also granted MEC.
2154 M. Clavero
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Supporting Information
Additional Supporting Information may be found in
the online version of this article:
Table S1. List of the 167 freshwater fish species
included in the analysis.
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(Manuscript accepted 26 May 2011)