Invasion patterns in riparian habitats: The role of anthropogenic pressure in temperate streams

Abstract

The riparian flora and the level of invasion in rivers of the Cantabric watershed in Spain were studied in relation to the ecological status and the anthropogenic pressure. The level of invasion was also analyzed in different riparian habitats: forests, river bars and man-made slopes. For this purpose 18 sites were sampled and a list of native and alien plant species was made along a 100-metre strip at each site. The habitat/s where alien species were found and their abundance per habitat and in the total area were also indicated. Out of 112 alien taxa found, 51 were classified as invasive. Exotic plants native to America were the most common (35%). The level of invasion was significantly higher in the sampling sites subject to high levels of hydrological and morphological disturbances, proxies of the anthropogenic pressure. River bars and man-made slopes supported similar number of alien plant species, higher than forests. We suggest that disturbance in river banks should be minimized as much as possible in order to diminish the risk of invasion.

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Invasion patterns in riparian habitats: The role of
anthropogenic pressure in temperate streams
D. Liendo
a
, I. Biurrun
a
, J. A. Campos
a
, M. Herrera
a
, J. Loidi
a
& I. García-Mijangos
a
a
Department of Plant Biology and Ecology, University of the Basque Country (UPV/EHU),
Spain
Accepted author version posted online: 09 Jul 2013.Published online: 13 Aug 2013.
To cite this article: Plant Biosystems - An International Journal Dealing with all Aspects of Plant Biology (2013):
Invasion patterns in riparian habitats: The role of anthropogenic pressure in temperate streams, Plant Biosystems - An
International Journal Dealing with all Aspects of Plant Biology: Official Journal of the Societa Botanica Italiana, DOI:
10.1080/11263504.2013.822434
To link to this article: http://dx.doi.org/10.1080/11263504.2013.822434
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Invasion patterns in riparian habitats: The role of anthropogenic
pressure in temperate streams
D. LIENDO, I. BIURRUN, J. A. CAMPOS, M. HERRERA, J. LOIDI, & I. GARCI
´
A-MIJANGOS
Department of Plant Biology and Ecology, University of the Basque Country (UPV/EHU), Spain
Abstract
The riparian flora and the level of invasion in the rivers of the Cantabric watershed in Spain were studied in relation to the
ecological status and the anthropogenic pressure. The level of invasion was also analyzed in different riparian habitats:
forests, river bars and man-made slopes. For this purpose, 18 sites were sampled and a list of native and alien plant species
was made along a 100-m strip at each site. The habitat/s where alien species were found and their abundance per habitat and
in the total area were also indicated. Out of 112 alien taxa found, 51 were classified as invasive. Exotic plants native to
America were the most common (35%). The level of invasion was significantly higher in the sampling sites subject to high
levels of hydrological and morphological disturbances, proxies of the anthropogenic pressure. River bars and man-made
slopes supported similar number of alien plant species, higher than forests. We suggest that disturbance in river banks should
be minimized as much as possible in order to diminish the risk of invasion.
Keywords: Alien plant, invasion level, river ecosystem, habitat, anthropogenic pressure, river quality index
Biological invasions have been chronicled at least for
two last centuries. However, it was not until the
initiation of the Scientific Comm ittee on Problems of
the Environment (SCOPE) in 1983 that the modern
field of invasion biology really began to take shape
(Richardson & Pys
ˇ
ek 2006; Davis 2011). There is
compelling evidence, based on global trade and
movement patterns, that the magnitude of this threat
is incr easing globally (Hulme 2009; McGeoch et al.
2010). Alien or exotic spe cies are often described as
one of the primary threats to ec osystems due to their
negative impact on native species diversity (Pimm
et al. 1995; Celesti-Grapow et al. 2010) and
ecosystem function (Vitousek et al. 1997).
Not all regions, biomes, or habitats are invaded to
the same extent. In fact, within a particular region
the level of invasion usually varies strongly among
habitats (Crawley 1987; Chytry
´
et al. 2008b),
suggesting that some habitats are more susceptible
to invasions than others. Differences in the level of
invasion among habitats depend on species traits
compared with native species, environmental and
biotic characteristics of the recipient habitat and the
propagule pressure with which alien species enter
into the recipien t habitat (Rejma
´
nek et al. 2005; Vila
`
et al. 2007; Stanisci et al. 2010).
Riparian ecosystems are among the most hum an-
altered e cosystems worldwide (Allan & Flecker
1993). They are considered to be highly prone to
invasion by alien plants, largely because of their
dynamic hydrology, their role as conduits for efficient
propagule dispersal, their human-driven degra-
dation, their nutrient and water conditions and the
intense disturbance regimes they exper ience (Hood
& Naiman 2000; Cushman & Gaffney 2010). The
expansion of exotic plants in these ecosystems was
accelerated when anthropogenic alterations such as
channel modifications and flow regulation or
drainage were int ensified. Moreover, the agricultural
wastewaters have increased the eutrophication of
these habitats and thus favoured the colonization by
alien species (Celesti-Grapow et al. 2010). Some of
these alien species may be present in large quantities,
so they can cause deep alterations both of floristic
composition and of vegetation an d soil struct ure
(Urgenson et al. 2009; Poldini et al. 2011). Riparian
areas often show the highest number of neophytes of
all natural and semi-natural vegetation types, as some
q 2013 Societa
´
Botanica Italiana
Correspondence: J. Loidi, Department of Plant Biology and Ecology, University of the Basque Country (UPV/EHU), Apdo. 644, E-48080 Bilbao, Spain.
Tel: þ 34 946015497. Fax: þ 34 946013500. Email: javier.loidi@ehu.es
Plant Biosystems , 2013
http://dx.doi.org/10.1080/11263504.2013.822434
Downloaded by [Universidad Del Pais Vasco], [Juan Antonio Campos] at 08:14 18 August 2013

studies conducted in Central Europe state (Pys
ˇ
ek
et al. 2002; Walter et al. 2005; Pys
ˇ
ek et al. 2010).
This high invasion level is an extremely alarming
issue, taking into account that riparian ecosystems
are considered of high ecological and economical
value. In fact, most riparian habitats have been
included in the European Habitat Directive (Euro-
pean Commission DG Environment 2003) due to
their priority interest for cons ervation.
A great progress has been made in the Iberian
Peninsula towards the knowledge of the alien flora
(Sanz-Elorza et al. 2004; Almeida & Freitas 2006;
Romero 2007; Campos & Herrera 2009b); however,
only a few studies have analyzed the plant invasion
across habitats (Vila
`
et al. 2007; Campos et al. 2013).
Some studies have focused on the assessment of plant
invasion in particular vegetation types, such as
coastal habitats in the North of Spain (Campos
et al. 2004; Can
˜
o et al. 2013) and riparian habitats in
Portugal (Aguiar et al. 2001, 2006, 2007) and
southern Spain (Tabacchi et al. 1996). Regarding
riparian habitats, riverine forests (Biu rrun et al.
1994; Biurr un et al. 2013) and herbaceous veg-
etation of river bars (Amigo 2006; Biurrun et al.
2008) have been studied in depth in the North of the
Iberian Peninsula; however, the impact of alien
species in these riparian habitats has not been
analyzed yet.
In this study, we hav e selected riparian ecosystems of
a temperate area to test whether the lev el of inv asion is
related to human activity and type of habitat. The
following objectives were proposed: (1) to identify the
alien plants present in the rivers of the Cantabric
watershed and their categories of invasion; (2) to
calculate the level of invasion of these rivers; (3) to
analyze the level of invasion in relation to the ecological
status and anthropogenic pressure of the rivers; and (4)
to determine which riparian habitats are the most
inv aded.
Materials and methods
Study area
The study was conducted in river basins of Bizkaia
and Gipuzkoa (Basque Country, Spai n) (Figure 1),
belonging to the Cantabrian–Basque biogeographic
sector and the Atlantic European province (Rivas-
Martı
´
nez 2007).
Temperature and rainfall in this territory are
homogeneous and highly influenced by its location
on the eastern coast of the Bay of Biscay. Overall, the
climate is described as temperate oceanic. Mean
annual precipitation varies from 1200 to 1700 mm
and mean annual temperature varies from 138Cto
148C. Most sampling points are located in meso-
temperate humid areas (Loidi et al. 2011).
The studied rivers belong to the Cantabr ic
watershed. All river basins show a great variety of
lithological substrata, with areas ranging from 100 to
1800 km
2
(Table I). River length varies from 15 to
70 km because their sources in the Cantabrian
Mountains and their mouths in the Bay of Biscay are
very close. The pronounced slopes they overcome,
along with the rainfall pattern, result in these rivers
showing torrential regimes, except in the final reaches
where valleys widen and wat er velocity decreases. In
addition to this, a slight flow reduction occurs during
summer due to a decrease in precipitation.
Riparian vegetation in all of the rivers studied
corresponds to the Cantabrian–Basque fluvial geo-
series, which is mainly constituted by alder forests
[Alnus glutinosa (L.) Gaertn.] (Loidi et al. 2011). Ash
(Fraxinus excelsior L.) and white willow (Salix alba L.)
forests can sometimes be found in the upper reaches
and near the river beds, respectively. River bars are
colonized by several herbaceous communities, such as
therophytic hygronitrophilous communities formed by
P olygonum sp . pl. and Bidens sp. pl., flooded grasslands
with Paspalum distichum and forb communities with
Figure 1. Study area and sampling sites.
D. Liendo et al.2
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Mentha sp. pl. Finally , aquatic and helophytic commu-
nities may develop associated with river beds where
water is always available and flow velocity slows down.
Sampling design and data collection
A total of 18 sites corresponding to the Ecological
Status Monitoring Network of the Basque Country’s
Rivers were studied (Department of Environment,
Basque Government) (Table I).
This monitoring network was used because of the
availability of data regarding the conservation status
and water quality of the rivers. Information on
different variables was taken from the monitoring
network of Basque rivers (Gartzia de Bikun
˜
a et al.
2008). Those variables were as follows: chemical
status [by means of the general quality index (ICG)]
and QBR index (riverbank forest quality index) as
proxies for the ecological status, and human-driven
hydrological and mor pholog ical disturbances as
proxies for the anthropogenic pressure.
The ICG index (Gartzia de Bikun
˜
a et al. 2008) is
based on the index of bacteriological and physico-
chemical quality developed by the Ministry of
Environment of Quebec (Canada) (He
´
bert 1997).
The calculation of this index takes into account
different parameters, such as pH, conductivity,
oxygenation, nutrients and metals. It ranges from 0
(ver y bad c hemical quality) to 100 (excellent
chemical quality). The QBR index (Munne
´
et al.
2003) is an index used to assess the quality of the
riverbank systems which integrates biological and
morphological aspects, such as vegetation quality,
diversity, structure and cover and river channel
condition. It ranges from 0 (extreme degrad ation,
bad quality) to 100 (riparian habitat in natural
condition). Disturbances related to water regulation,
extraction and diversion were considered as hydro-
logical disturbances; four categories had been
distinguished (Garcı
´
a de Bikun
˜
a et al. 2008): no
disturbance and low, medium and high disturbances.
Finally, morphological disturbances included weirs,
bridges, breakwaters and other occupations of the
Public Hydraulic Domain, with three categories: low,
medium and high (Garcı
´
a-Bikun
˜
a et al. 2008).
Data coll ection was done from 2008 to 2010
during the period of maximum development of the
riparian vegetation (i.e. between June and Septem-
ber). A 100-m strip upstream of each point was
sampled (Aguiar et al. 2007). The strip’s width
depended on the perifluvial environment, which was
in turn influence d by the geomorphology and the
river stretch itself. We consider this sampled area to
be representative for the study as it usually includes
all type of habitats present in the Cantabric rivers. A
list of native and alien plants present in the area was
compiled. The abundance of alien species per habitat
and in the total area were quantified by means of a 9-
index scale (Braun-B lanquet 1951): r (punctual); þ
(, 1%); 1 (1–5%); 2a (5 –10%); 2b (10 – 20%); 2c
(20–25%); 3 (25 – 50%); 4 (50 – 75%); 5 (75–
100%). Five habitat types were considered: forests,
river bars, man-made slopes, terraces and helophytic
communities. Forests gather all type of tree
formations, provided tree cover is . 50%. River
bars include all type of herbaceous communities
developing on sand, mud or gravel bars in river beds,
e.g. flooded grasslands, nitrophilous therophytic
communities and forb communities. Man-made
slopes are degraded river banks, breakwaters and
Table I. Sampling sites and variables used in the analyses.
No. Site River Basin Basin area (km
2
) LI ICG QBR HD MD
1 B226 Butro
´
n Butro
´
n 172.2 9.5 69.9 25 No Medium
2 BI555 Bidasoa Bidasoa 700 15.6 80.8 40 Medium Medium
3 DEG068 Ego Deba 530.3 23.2 56.6 30 Medium High
4 G082 Gobela Ibaizabal 1798.8 29.3 72.3 30 No High
5 I271 Ibaizabal Ibaizabal 1798.8 15.5 72.6 15 No High
6 KA326 Cadagua Ibaizabal 1798.8 14.8 70.2 25 Medium High
7 KA517 Cadagua Ibaizabal 1798.8 25.7 70.6 35 Low High
8 L196 Lea Lea 99.3 11.6 79.1 65 No Low
9 M045 Barbadu
´
n Barbadu
´
n 128.9 3.8 72.0 100 No Medium
10 M190 Barbadu
´
n Barbadu
´
n 128.9 17.6 78.2 70 No High
11 N520 Nervio
´
n Ibaizabal 1798.8 41.1 73.9 5 Low High
12 NA260 Altube Ibaizabal 1798.8 19.8 78.1 60 Medium Medium
13 NZ124 Zeberio Ibaizabal 1798.8 13.1 78.8 30 No Medium
14 O262 Oria Oria 882 22.6 75.9 20 Medium High
15 OK045 Oka Oka 183.2 9.2 78.1 30 No Medium
16 OKMA040 Mape Oka 183.2 9.4 82.3 40 No High
17 U490 Urola Urola 342.2 18.3 71.0 50 Low Low
18 UR320 Urumea Urumea 272.4 8.3 81.9 35 High Medium
Note: LI, level of invasion; ICG, general quality index; QBR index, riverbank forest quality index; HD, hydrological disturbances; MD,
morphological disturbances.
Invasion patterns in riparian habitats 3
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walls colonized by ruderal communities. Ter races
include different kinds of grasslands and f orb
communities developing in the river terrace, and
helophytic communities are those formed by species
adapted to the water–land ecotone, such as reed,
Phragmites australis.
Floristic data
Several sources were used for the identification and
nomenclature of native and alien taxa: general floras
(Castroviejo et al. 1986 –2012; Aizpuru et al. 1999)
and different monographs.
Information regarding category of invasion and
geographical origin of alien plants was taken from
Campos and Herrera (2009b) and Campos (2010).
We have considered the categories of invasion
proposed by Richardson et al. (2000), wh o recog-
nized four categories: invasive transformer (A),
invasive non-transformer (B), naturalized (C) and
casual (D). In addition, we have included a new
category for those species whose native or alien status
is not clear (E) (Campos & Herrera 2009b). The
latter were cons idered as alien species in the analyses.
Regarding geographical origin, those plants that
were not possible to identify at species level, hybrids
and species of unknown geographical origin were
included in the category “other” (Table S1).
Data analysis
The level of invasion was calculated as the proportion
of alien plant species in relation to the total number of
species (Chytry
´
et al. 2008a). This ratio has been
proposed by Catford et al. (2011) with the name
“relative alien species richness” as a recommended
way to calculate the level of invasion, independ ent of
sampling plot size. The original categoric al variables
for the hydrological and mor phological disturbances
of the rivers were recodified for the statistical analysis
due to the low number of cases for some of the
variables (see Table I). Two categorical variables were
finally established as follows: no disturbance and
disturbance (including low, medium and high) for
human-driven hydrological dis turbances, and high
and medium/low for morphological disturbances.
Non-parametrical Mann –Whitney’s U-test was
used to analyze the level of invasion and the numbe r
of alien and native species in relation to the
hydrological and morphological disturbances
because data were qualitative and did not show a
nor mal distr ibution. Bivariate correlations were used
for the chemical status and the QBR index because
quantitative data were available. All statistical
analyses were carried out using SPSS statistics 19.0
package.
Results
Categories of invasion and geographical origin of the alien
flora
A total of 112 alien plant taxa were found in the
sampled rivers. These species are listed in Table S1,
which includes the family, category of invasion,
geographical orig in, fluvial h abitat/s where the
species were found, the number of sites where the
species occurred and the mean cover of the species in
those sites where they were present.
Considering the category of invasion (Figure 2(A)),
almost half of the alien species found in the rivers of the
Cantabric watershed were invasive (51). Of these, 12
were classified as transformers (11%), such as Cyperus
eragrostis, Fallopia japonica and Robinia pseudoacacia,
and 39 as invasive non-transformers (34%), such as
Crocosmia £ crocosmiiflora and Platanus hispanica.
Figure 2. Percentage of alien plants in the Cantabric rivers. (A)
The categor y of invasion and (B) the geographical origin.
D. Liendo et al.4
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In addition, 33 naturalized plants were also found
(29%), such as Ligustrum ovalifolium,alongwith25
casual species (22%) and 5 species whose native/alien
status is not clear (4%), such as Dorycnium rectum.
With regard to the geographical origin (Figure 2
(B)), 41 taxa, such as Amaranthus sp. pl., Conyza
sp. pl., Cyperus eragrostis, Paspalum distichum, Robinia
pseudoacacia and Tradescantia fluminensis, were native
to America, representing the highest proportion
(35%). Asian species, such as Buddleja davidi i,
Fallopia japonica and Ligustrum ovalifolium, were
quite common as well (19 species), representing 17%
of the total, whereas species from Africa, Europe, the
Mediterranean basin and Australia were less numer-
ous – 5 (4%), 4 (4%), 10 (9%) and 2 (2%),
respectively. There were also a high number of alien
plants belonging to the category “other” (25).
Level of invasion
Overall, the level of invasion was higher in the sites
situated on industrial and very populated areas
(Table I), with values ranging from 20% to 30%
except in the Nervio
´
n river near Bilbao (N520)
where the level of invasion was even higher (41%).
Lowest value (4%) was obtained in the site M045,
located in the upper stretch of Barbadu
´
n stream that
flows through a mountainou s valley with low
population density. No longitudinal pattern was
found along an east –west gradient, but the level of
invasion tended to increase downstream.
Level of invasion versus ecological status and
anthropogenic pressure
Chemical status (by means of the ICG index) and
QBR index as proxies for the ecological status, and
hydrological and morphological disturbances
(proxies for the anthropogenic pressure) were
analyzed with regard to the level of invasion and
the number of native and alien species in order to
find out whether there were any differences among
them.
A slight negative correl ation was found between
the QBR index and the level of invasion (r ¼ 0.235;
p , 0.05). Regarding chemical status, the ICG index
is slightly correlated with the number of native
species (r ¼ 0.241; p , 0.05), but not with the level
of invasion or the number of alien taxa. With respect
to hydrological disturbances, Mann –Whitney’s U-
test revealed that there were significant diffe rences in
the number of alien species and the level of invasion
[ p , 0.05, see Figure 3(A),(B)], with higher values
in those sites subject to some kind of hydrological
disturbance. An increase in the number of native
species is also shown, although it is not significant
(Table II). Finally, Mann–Whitney’s U-test also
pointed out that there were significant differences in
the level of invasion [ p , 0.05, see Figure 3(C)]
between both categories of morphological disturb-
ances, with higher values in those sites subject to a
high degree of disturbance. In this case, the number
of alien species also increases, whereas the number of
native taxa decreases (Table II), although not in a
significant manne r.
Alien plants and riparian habitats
Forests, river bars and man-made slopes are the most
common riparian habitats in the rivers of the
Cantabric water shed. Terraces and helophytic com-
munities are very scarce due to the geomorphology of
these rivers, and they were not taken into account
because the low number of sites where those habitats
occurred did not allow us to carry out an appropriate
assessment.
River bars and slopes supported a similar number
of alien plant species (68 and 65, respectively) and
Figure 3. Box-plot diagrams showing the relation between the plant invasion and the anthropogenic disturbance. (A) Relationship between
the number of alien species and the hydrological disturbance, (B) relationship between the level of invasion and the hydrological disturbance
and (C) relationship between the level of invasion and the morphological disturbance. The boxes represent the interquartile range, the thick
line indicates the median, the bars show the values range that accounts for 95% of the cases and circles represent outliers.
Invasion patterns in riparian habitats 5
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notably more than forests (46). Overall, these
differences were due to a higher presence of invasive
non-transformer plants (category B, see Figure 4), as
the number of spe cies of the remaining categories did
not show an important variation.
In riparian forests, Platanus hispanica and Robinia
pseudoacacia were the most remarkable alien species
in the tree layer, both of them present in eight sites,
with mean coverage of 20% and around 15%,
respectively. In the herb layer, Tradescantia fluminen-
sis and Crocosmia £ crocosmiiflora are also worth
mentioning. Although T. fluminensis showed a higher
mean coverage (5%) than C. £ crocosmiiflora (3%),
the latter was more frequent, being present in eight
sites.
On river bars, Cyperus eragrostis was the most
frequent alien species, being present in 12 sites, with
a m ean coverage around 4% in this habitat. Paspalum
distichum showed the highest mean coverage (15%)
in the 11 sites where it was present indicating the
great invasion success this species has in this habitat.
Other species with high frequency on river bars were
Bidens fron dosa (in four sites) and Amaranthus sp. pl.
(in seven sites); however, the mean coverage in both
cases was , 1%.
On man-made slopes, Fallopia japonica was one of
the most prominent species. Even though it was only
found in four sites, its mean coverage was around
15% in this man-made habitat, showing therefore a
great invasive character that could cause significant
problems if spread to other river basins. Other
noteworthy s pecies on man-made slopes were
Dorycnium rectum, present in six sites with a mean
coverage of 5%, and Buddleja davidii, found in four
sites with a mean coverage around 4%.
Discussion
Invasive plants (transformer s and non-transformers)
represent almost half of the Cantabric riparian alien
flora [44%, see Figure 2(A)]. This percentage is
remarkably higher than that obtained for Bizkaia’s
riparian habitats (31.2%) in a study that covered
different habitats of this territory (Campo s & Herrera
2009a); it is necessary to highlight that the number of
invasive non-transformer plant species (B) rises from
16 in the aforementioned study to 38 in this study.
This could be due to the fact that this study focused
exclusively on ripar ian systems, with a subsequent
more extensive sampling which revealed a major
presence of the invasive component of the alien flora.
The high proportion of invasive plants could be the
outcome of the mild climate of the study area along
with the level of disturbance of the rivers, which
would facilitate the establishment of strong invaders.
An important proportion of the alien plant species
found in the studied rivers is native to America (39%),
followed by those of Asian origin (16%). These
percentages are similar to those obtained for the
province of Bizkaia (Campos & Herrera 2009a),
pointing out that the trend would be the same for the
rivers. However, the percentage of Mediter ranean
species (9%) has been notably low, probably due to
the hygrophilous character of riparian habitats.
The highest level of invasion (around 20–30%)
was found in those river basins subject to the highest
level of anthropogenic pressure and in general it
coincides with a low QBR index. These river basins
are situated in industrialized and densely populated
areas, which could facilitate the arrival and sub-
sequent establishment of alien plant species. This
level of invasion is similar to that obtained in other
studies carried out in rivers of similar climatic and
Table II. Native and alien species richness in relation to hydrological and morphological disturbance.
Native species Alien species
Median IQR Median IQR
Hydrological disturbance No disturbance 77 65– 89 13 8–17
Disturbance 84 76– 122 24 17–29
Morphological disturbance Medium/low 113 75– 128 13 8–17
High 77 69– 84 23 15–27
Note: IQR, interquartile range.
Figure 4. Number of alien plant species in the main riparian
habitats regarding their category of invasion. (A) Transformer, (B)
invasive non-transformer, (C) naturalized, (D): casual and (E)
unclear.
D. Liendo et al.6
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biogeographic conditions, such as the Adour (24 %)
and Garonne (21%) in south-west France (Planty-
Tabacchi et al. 1996; Tabacchi & Planty-Tabacchi
2005). However, the patterns of invasion of the
Cantabric rivers are different to those observed in the
French rivers, where the highest pro portion of exotic
species was found in areas with intermediate
disturbance l evel. Other stud ies cond ucted in
Mediterranean rivers of Portugal (Aguiar et al.
2001) and south-east Spain (Salinas & Casas 2007)
showed a similar pattern to our Cantabric rivers, with
higher invasion values being found in sites subject to
a high level of anthropogenic pressure; although the
level of invasion was in general lower in those
Mediterranean rivers.
Even though the level of invasion increases with
both hydrological and morphological disturbances,
only the latter negatively affects native species
richness. Should hydrological disturbances occur,
the number of native and, more markedly, alien
species increases. Thus, many alien plants as well as
native ruderals may be favoured by natural and
anthropogenic hydrological disturbances (Planty-
Tabacchi et al. 1996). Nevertheless, further disturb-
ance or river regulation by higher human pressure
could cause the loss of spatial complexity and thus
could open the door to some dominant invaders,
with drastic consequences on biodiversity (Tabacchi
& Planty-Tabacchi 2005). This fits well with our
obser vations in Cantabric river s, where highl y
disturbed places, with many morphological altera-
tions, are quite easily colonized by some dominant
invaders such as Fallopia japonica.
Not only is the invasion level similar in Cantabric
rivers and in the Adour and Garonne rivers in south-
west France, but they also share many of the alien
species, some of which are i nvasive and very
common. Among them, Acer negundo, Robinia
pseudoacacia and Buddleja davidii as woody species
and Cyperus eragrostis, Bidens frondosa, Paspalum
distichum and Fallopia japonica as herbaceous taxa are
worth highlighting. Nevertheless, some invasive
plants in Cantabric rivers such as Solanum chenopo-
dioides and Crocosmia £ crocosmiiflora are not
important in the French rivers.
The level of invasion in some river basins such as
the Barbadu
´
n and Ibaizabal tended to increase
downstream, a pattern also found in other rivers
(Planty-Tabacchi et al. 1996; Tabacchi et al. 1998)
and that has been primarily related to the increas-
ingly mild climate and greater human impact towards
the lower valleys.
River bars and man-made slopes are the riparian
habitats supporting higher number of alien plant
species. Human-dr iven alterations and frequent
natural flood disturbance on man-m ade slopes and
river bars help to create open gaps with light,
nutrients and space that can be rapidly colonized by
ruderal species, many of them alien plants (Walter
et al. 2005; Richardson et al. 2007).
Further insights
Concerning management of plant invasions, although
the level of invasion is the basic issue, it can be
complemented with information about alien transfor-
mer species (Catford et al. 2011). Among the invasive
transformers present in Cantabric rivers, one of the
most dangerous to be taken into account in the scope of
biological conservation is Fallopia japonica (Gerber
et al. 2008). This Asiatic species has been reported as
invasive in Central and Northern Europe since the
19th century, where it has become very dangerous for
the fluvial environment (Pys
ˇ
ek 2009). Attempts to
control and eradicate Fallopia japonica have been
carried out in some Cantabric rivers. Mechanical
removal and the use of herbicides have been the most
widespread treatments to date. However, no results are
available at the moment regarding the long-term
effectiveness of those treatments.
The high economical costs, lack of public
awareness and support and absence of coordination
among different public admin istrations (Andreu
et al. 2009) difficult the control and eradication of
invasive species. In our opinion, the best way to fight
against plant invasion is prevention, and the most
important actions should be (1) to limit the source of
new propagules, (2) to minimize hydrological and
morphological disturbances and (3) to maintain and
restore riparian forests. Moreover, the first detection
is crucial for eradication success because it prevents
further population growth and spread (Pluess et al.
2012). Thus, this type of survey is very important not
only to improve the knowledge about the ecology and
distribution of alien species but also to detect new
future invasions.
Acknowledgements
Funds from the projects IT299-10 for research
groups of the Basque Government, CGL2009-
13317-C03-02 of the Spanish Ministry of Science
and Innovation and Ca
´
tedra UNESCO o f the
University of the Basque Country UPV/EHU 17/91
have been used for this survey.
References
Aguiar FC, Ferreira MT, Albuquerque A. 2006. Patterns of exotic
and native plant species richness and cover along a semi-arid
Iberian river and across its floodplain. Plant Ecol 184:
189–202.
Aguiar FC, Ferreira MT, Albuquerque A, Moreira I. 2007. Alien
and endemic flora at reference and non-reference sites in
Invasion patterns in riparian habitats 7
Downloaded by [Universidad Del Pais Vasco], [Juan Antonio Campos] at 08:14 18 August 2013

Mediterranean-type streams in Portugal. Aquat Conserv Mar
Freshwater Ecosyst 17: 335 –347.
Aguiar FC, Ferreira MT, Moreira I. 2001. Exotic and native
vegetation establishment following channelization of a western
Iberian river. Regul Rivers Res Manage 17: 509 –526.
Aizpuru I, Aseginolaza C, Uribe-Echebarrı
´
a PM, Urrutia P,
Zorrakin I, editors. 1999. Claves ilustradas de la flora del Paı
´
s
Vasco y territorios limı
´
trofes [Ilustrated keys for the flora of the
Basque Country and bordering territories]. Vitoria-Gasteiz:
Servicio Central de Publicaciones del Gobierno Vasco.
Allan JD, Flecker AS. 1993. Biodiversity conservation in running
waters. Bioscience 43: 32– 43.
Almeida JD, Freitas H. 2006. Exotic naturalized flora of
continental Portugal – A reassessment. Bot Complutensis 30:
117–130.
Amigo J. 2006. Los herbazales terofı
´
ticos higronitro
´
filos en el
noroeste de la Penı
´
nsula Ibe
´
rica [Therophytic hygronitrophi-
lous tall-herb communities in northwestern Iberian Peninsule]
(Bidentetea tripartitae Tu
¨
xen, Lohmeyer & Preising ex von
Rochow 1951). Lazaroa 27: 43 –58.
Andreu J, Vila
`
M, Hulme PE. 2009. An assessment of stakeholder
perceptions and management of noxious alien plants in Spain.
Environ Manage 43: 1244 –1255.
Biurrun I, Campos JA, Herrera M, Loidi J, Garcı
´
a-Mijangos I.
2013. A survey of the riverine forests of the northern Iberian
Peninsula: Numerical classification versus traditional syntax-
onomy and relationships with climatic gradients. Doc Phytosoc
(accepted).
Biurrun I, Garcı
´
a-Mijangos I, Crespo MB, Ferna
´
ndez-Gonza
´
lez F.
2008. Los herbazales higronitro
´
filos de Epilobium hirsutum y
Mentha longifolia en los curs os fluviales de la Penı
´
nsula Ibe
´
rica
[Hygronitrophilous forb communities dominated by Epilobium
hirsutum and Mentha longifolia in riparian habitats from the
Iberian Peninsula]. Lazaroa 29: 69–86.
Biurrun I, Garcia-Mijangos I, Loidi J. 1994. Study of alder forests
in the Basque Country and bordering territories by means of
multivariate analysis. Bot Helv. 104(1): 31–54.
Braun-Blanquet J. 1951. Pflanzensoziologie. Grundzu
¨
ge der
Vegetationskunde [Phytosociology. Basic features of Vegetation
Science]. Wien: Springer.
Campos JA. 2010. Flora alo
´
ctona del Paı
´
s Vasco y su influencia en
la vegetacio
´
n [Alien flora of the Basque Country and its impact
on vegetation] [Ph. D. dissertation]. Leioa, BI: University of
the Basque Country UPV/EHU. p.484.
Campos JA, Biurrun I, Garcı
´
a-Mijangos I, Loidi J, Herrera M.
2013. Assessing the level of plant invasion: A multi-scale
approach based on vegetation plots. Plant Biosyst. (in press).
Campos JA, Herrera M. 2009a. Ana
´
lisis de la flora alo
´
ctona de
Bizkaia (Paı
´
s Vasco, Espan
˜
a) [Analysis of the alien flora of
Bizkaia (The Basque Country, northern Spain)]. Lazaroa 30:
7– 33.
Campos JA, Herrera M. 2009b. Diagnosis de la Flora alo
´
ctona
invasora de la Comunidad Auto
´
noma del Paı
´
sVasco
[Diagnosis of the Invasive Alien Flora in the Basque Country].
Bilbao: Gobierno Vasco.
Campos JA, Herrera M, Biurrun I, Loidi J. 2004. The role of alien
plants in the natural coastal vegetation in central-northern
Spain. Biodivers Conserv 13: 2275 –2293.
Can
˜
o L, Campos JA, Garcı
´
a-Magro D, Herrera M. 2013.
Replacement of estuarine communities by an exotic shrub:
Distribution and invasion history of Baccharis halimifolia in
Europe. Biol Invasions 15: 1183 –1188.
Castroviejo S (coord. gen.). 1986– 2012. Flora iberica: Plantas
vasculares de la Penı
´
nsula Ibe
´
rica e Islas Baleares[Flora Iberica:
Vascular Plants of the Iberian Peninsula and Balearic Islands].
1– 8, 10– 15, 17– 18, 21 vols. Madrid: Real Jardı
´
n Bota
´
nico,
CSIC.
Catford JA, Vesk PA, Richardson DM, Pys
ˇ
ek P. 2011. Quantifying
levels of biological invasion: Towards the objective classifi-
cation of invaded and invasible ecosystems. Global Change
Biol 18: 44– 62.
Celesti-Grapow L, Alessandrini A, Arrigoni PV, Assini S, Banfi E,
Barni E, et al. 2010. Non-native flora of Italy: Species
distribution and threats. Plant Biosyst 144: 12–28.
Chytry
´
M, Jaros
ˇ
ik V, Pys
ˇ
ek P, Ha
´
jek O, Knollova
´
I, Tichy
´
L, et al.
2008a. Separating habitat invasibility by alien plants from the
actual level of invasion. Ecology 89: 1541– 1553.
Chytry
´
M, Maskell LC, Pino J, Pys
ˇ
ek P, Vila
`
M, Font X, et al.
2008b. Habitat invasions by alien plants: A quantitative
comparison among Mediterranean, subcontinental and ocea-
nic regions of Europe. J Appl Ecol 45: 448–458.
Crawley MJ. 1987. What makes a community invasible? In: Gray
AJ, Crawley MJ, Edwards PJ, editors. Colonization, succession
and stability. Oxford: Blackwell. pp. 429–543.
Cushman JH, Gaffney KA. 2010. Community-level consequences
of invasion: Impacts of exotic clonal plants on riparian
vegetation. Biol Invasions 12: 2765–2776.
Davis MA. 2011. Researching invasive species 50 years after Elton:
A cautionary tale. In: Richardson DM, editor. Fifty years of
invasion ecology: The legacy of Charles Elton. Oxford:
Blackwell. pp. 269–276.
European Commission DG Environment. 2003. Interpretation
manual of European Union Habitats – EUR 25. Brussels:
European Commission DG XI.
Gartzia de Bikun
˜
a B, Agirre A, Arrate J, Blanco JM, Fraile H,
Lapaza J, et al. 2008. Red de Seguimiento del Estado Ecolo
´
gico
de los Rı
´
os de la Comunidad Auto
´
noma del Paı
´
s Vasco. 2007
[Monitoring network for the ecological status of the rivers in
the Basque Country. 2007]. Informe de la UTE Anbiotek-
Ondoan para la Agencia Vasca del Agua.
Gerber E, Krebs C, Murrell C, Moretti M, Rocklin R, Schaffner
U. 2008. Exotic invasive knotweeds (Fallopia sp.) negatively
affect native plant and invertebrate assemblages in European
riparian habitats. Biol Conserv 141: 646–654.
He
´
bert S. 1997. De
´
velopement d’un indice de la qualite
´
bacte
´
riologique et physico-chimique de l’eau pour le0s rivie
`
res
du Que
´
bec [Development of a bacteriological and physico-
chemical quality index for the rivers of Que
´
bec]. Que
´
bec:
Ministe
`
re de l’Environnement et de la faune.
Hood GW, Naiman RJ. 2000. Vulnerability of riparian zones to
invasion by exotic vascular plants. Plant Ecol 148: 105 –114.
Hulme PE. 2009. Trade, transport and trouble: Managing invasive
species pathways in an era of globalization. J Appl Ecol 46:
10– 18.
Loidi J, Biurrun I, Campos JA, Garcı
´
a-Mijangos I, Herrera M.
2011. La vegetacio
´
n de la Comunidad Autono
´
ma del Paı
´
s
Vasco. Leyenda del mapa de series de vegetacio
´
n a escala
1:50.000. Leioa: University of the Basque Country UPV/EHU.
McGeoch MA, Butchart SHM, Spear D, Marais E, Kleynhans EJ,
Symes A, et al. 2010. Global indicators of biological invasion:
Species numbers, biodiversity impact and policy responses.
Divers Distrib 16: 95 –108.
Munne
´
A, Prat N, Sola
`
C, Bonada N, Rieradevall M. 2003. A
simple field method for assessing the ecological quality of
riparian habitat in rivers and streams: QBR index. Aquat
Conserv Mar Freshwater Ecosyst 13: 147 –163.
Pimm SL, Russell GJ, Gittelman JL, Brooks TM. 1995. The
future of biodiversity. Science 269: 347 –350.
Planty-Tabacchi AM, Tabacchi E, Naiman RJ, Deferrari C,
De
´
camps H. 1996. Invasibility of species rich communities in
riparian zones. Conserv Biol 10: 598 –607.
Pluess T, Cannon R, Jaros
ˇ
ik V, Pergl J, Pys
ˇ
ek P, Bacher S. 2012.
When are eradication campaigns successful? A test of common
assumtions. Biol Invasions 14(7): 1365– 1378.
D. Liendo et al.8
Downloaded by [Universidad Del Pais Vasco], [Juan Antonio Campos] at 08:14 18 August 2013

Poldini L, Vidali M, Ganis P. 2011. Riparian Salix alba: Scrubs of
the Po lowland (N Italy) from an European perspective. Plant
Biosyst 145: 132– 147.
Pys
ˇ
ek P. 2009. Fallopia japonica (Houtt.) Ronse Decr., Japanese
knotweed (Polygonaceae, Magnoliophyta). In: DAISIE, editor.
Handbook of alien species in Europe. Berlin: Sprin ger. p. 348.
Pys
ˇ
ek P, Bacher S, Chytry
´
M, Jaros
ˇ
ı
´
k V, Wild J, Celesti-Grapow L,
et al. 2010. Contrasting patterns in the invasions of European
terrestrial and freshwater habitats by alien plants, insects and
vertebrates. Global Ecol Biogeogr 19: 317 –331.
Pys
ˇ
ek P, Sa
´
dlo J, Manda
´
k B. 2002. Catalogue of alien plants of the
Czech Republic. Preslia 74: 97– 186.
Rejma
´
nek M, Richardson DM, Pys
ˇ
ek P. 2005. Plant invasions and
invasibility of plant communities. In: van der Maarel E, editor.
Vegetation ecology. Oxford: Blackwell. pp. 332– 355.
Richardson DM, Holmes PM, Esler KJ, Galatowitsch SM,
Stromberd JC, Kirkman P, et al. 2007. Riparian vegetation:
Degradation, alien plant invasions, and restoration prospects.
Divers Distrib 13: 126 –139.
Richardson DM, Pys
ˇ
ek P. 2006. Plant invasions: Merging the
concepts of species invasiveness and community invasibility.
Prog Phys Geogr 30: 409– 431.
Richardson DM, Pys
ˇ
ek P, Rejma
´
nek M, Barbour MG, Panetta
FD, West CJ. 2000. Naturalization and invasion of alien plants:
Concepts and definitions. Divers Distrib 6: 93 –107.
Rivas-Martı
´
nez S. 2007. Mapa de series, geoseries y geomicro-
series de vegetacio
´
ndeEspan
˜
a [Manual del mapa de
vegetacio
´
n potencial de Espan
˜
a]. Parte 1 [Series, geoseries
and geomicroseries map of Spain [Handbook for the potential
vegetation map of Spain]. Part I]. Itinera Geobot 17: 5 –435.
Romero I. 2007. Flora exo
´
tica de Galicia (Noroeste ibe
´
rico)
[Exotic flora of Galicia (Northwest Iberian Peninsula)]. Bot
Complutensis 31: 113– 115.
Salinas MJ, Casas J. 2007. Riparian vegetation of two semi-arid
Mediterranean rivers: Basin-scale responses of woody and
herbaceous plants to environmental gradients. Wetlands 27:
831–845.
Sanz-Elorza M, Dana ED, Sobrino E, editors. 2004. Atlas de las
Plantas Alo
´
ctonas Invasoras en Espan
˜
a [Atlas of Invasive Alien
Plants in Spain]. Madrid: Direccio
´
nGeneralparala
Biodiversidad.
Stanisci A, Acosta ATR, Di Iorio A, Vergalito M. 2010. Leaf and
root trait variability of alien and native species along Adriatic
coastal dunes (Italy). Plant Biosyst 144(1): 47–52.
Tabacchi E, Correll DL, Hauer R, Pinay G, Planty-Tabacchi AM,
Wissmar C. 1998. Development, maintenance and role of
riparian vegetation in the river landscape. Freshwater Biol 40:
497–516.
Tabacchi E, Planty-Tabacchi AM. 2005. Exotic and native plant
community distributions within complex riparian landscapes:
A positive correlation. Ecoscience 12: 412– 423.
Tabacchi E, Planty-Tabacchi AM, Salinas MJ, De
´
camps H. 1996.
Landscape structure and diversity in riparian plant commu-
nities: A longitudinal comparative study. Regul Rivers Res
Manage 12: 367–390.
Urgenson LS, Reichard SH, Halpern CB. 2009. Community and
ecosystem consequences of giant knotweed (Polygonum
sachalinense) invasion into riparian forests of western Washing-
ton, USA. Biol Conserv 142: 1536– 1541.
Vila
`
M, Pino J, Font X. 2007. Regional assessment of plant
invasions across different habitat types. J Veg Sci 18: 35 –42.
Vitousek PM, D’Antonio CM, Loope LL, Rejma
´
nek M,
Westbrooks R. 1997. I ntroduced species: A significant
component of human-caused global change. N Z J Ecol 21:
1– 16.
Walter J, Essl F, Englisch T, Kiehn M. 2005. Neophytes in Austria:
Habitat preferences and ecological effects. Neobiota 6: 13– 25.
Invasion patterns in riparian habitats 9
Downloaded by [Universidad Del Pais Vasco], [Juan Antonio Campos] at 08:14 18 August 2013