A-socialecological-system-framework-to-assess-biological-invasions-Corbicula-fluminea-in-Galicia-NW-Iberian-PeninsulaBiological-Invasions 2019

Biol Invasions (2019) 21:587–602
https://doi.org/10.1007/s10530-018-1846-5
(0123456789().,-volV)
(0123456789().,-volV)
ORIGINAL PAPER
A social-ecological system framework to assess biological
invasions: Corbicula fluminea in Galicia (NW Iberian
Peninsula)
Noé Ferreira-Rodrı́guez
. Omar Defeo . Gonzalo Macho . Isabel Pardo
Received: 16 January 2018 / Accepted: 12 September 2018 / Published online: 17 September 2018
Springer Nature Switzerland AG 2018
Abstract In this study we hypothesize that Ostrom’s
social-ecological system (SES) framework can be
useful to address the introduction pathways and
dispersal vectors of non-native species. We have
applied this framework to the introduction of the Asian
clam Corbicula fluminea in freshwaters in Galicia
(Spain). We reviewed scientific and grey literature and
performed a series of interviews with key stakeholders. This information, coupled with an extensive
survey campaign, provided an updated C. fluminea
distribution map. Using a Principal Component Analysis and pair-wise correlations we analyzed a set of 18
social, ecological, economic and governance variables
and related them to the total number of water bodies
invaded by C. fluminea in Galicia. Our field data on C.
fluminea distribution indicated a mean upstream
spread of 3.6 km yr-1. We suggest that the total
number of water bodies invaded by C. fluminea in
Electronic supplementary material The online version of
this article (https://doi.org/10.1007/s10530-018-1846-5) contains supplementary material, which is available to authorized
users.
N. Ferreira-Rodrı́guez (&) G. Macho I. Pardo
Departamento de Ecoloxı́a e Bioloxı́a Animal, Facultade
de Bioloxı́a, Campus As Lagoas – Marcosende,
Universidade de Vigo, 36310 Vigo, Spain
e-mail: [email protected]
O. Defeo
Faculty of Sciences, UNDECIMAR, Iguá 4225,
11400 Montevideo, Uruguay
Galician freshwaters is mainly linked to the following
variables of the social (higher education level and
mass media news), ecological (endangered freshwater
species, scientific publications, dams, wastewater
treatment plants, livestock, and agricultural lands),
economic (gross domestic product, gross imports, and
industrial productivity index) and governance
(surveillance, legislative instruments and non-governmental organizations) dimensions. The SES framework has been useful in identifying introduction
pathways and dispersal vectors of non-native species.
We encourage decision-makers to get involved in real
implementation of legislative instruments and management plans that will be benefitted by collaborating
efforts between stakeholders.
Keywords Non-native invasive species Management Recreational freshwater use Invasion
vectors SES framework
Introduction
Biological exchange has increased dramatically with
global trade since the 19th century (Cambray 2003;
Jeschke and Strayer 2005). In Europe, approximately
750 freshwater species reported as non-native are
estimated to have been introduced (EASIN 2018).
Europe’s Iberian Peninsula, specifically its Northern
123
588
region whose freshwater habitats are particularly
hospitable to new invaders, constitutes a ‘‘hot spot’’
for non-native invasive species (Maceda-Veiga et al.
2010). In this regard, rivers can act as transportation
networks for new introductions and subsequent spread
of non-native invasive species (Galil et al. 2007;
Leuven et al. 2009). Scientific evidence of the broad
geographic and taxonomic extent of species invasion
in freshwater environments is robust. Nevertheless,
the process for early detection of a potential nonnative invader to the publication of the first scientific
evidence and implementation of management strategies could take years or even decades.
Non-native invasive species are causing important
changes in communities and ecosystems (Gurevitch
and Padilla 2004). The threat of non-native species
clearly requires the implementation of preventive
strategies, because once a species is detected in the
recipient environment and the exponential growth
phase starts, little or nothing can be done to prevent
subsequent ecological, economic and social damage
(Sakai et al. 2001). Hence, the involvement of
different stakeholders to avoid the introduction of
non-native invasive species has been invoked as one of
the most effective tools in an early warning system
(Dehnen-Schmutz et al. 2010). Traditionally, research
efforts on non-native invasive species are focused on
the ecological dimension (i.e., relationship between
non-native invasive species and the environment). To
prevent new species introductions, management policies should consider both ecological and social
dimensions. In practice, management policies involve
the identification of the problem based on the invasive
potential of each species (i.e., ecological dimension)
(Maguire 2004), and are intended to avoid new
introductions and eradicate or control existing ones.
Some examples provide evidence of the effectiveness of institutional actions to address new introductions. For example, the chemical elimination (i.e.,
chlorine and copper sulfate) of the marine bivalve
black striped mussel [Mytilopsis sallei (Récluz 1849)]
from Australian tropical waters was one of the few
successful aquatic pest eradications undertaken in the
world (Ferguson 2000). Similarly, after scientific
concerns were raised about initial efforts to combat
the seaweed Caulerpa taxifolia on the American
Pacific coast, governmental agencies began an immediate eradication program (Williams and Schroeder
2004). More recently, in Europe, managers have
123
N. Ferreira-Rodrı́guez et al.
begun controlling the yellow-legged hornet Vespa
velutina Lepeletier, 1836, through collaborative
efforts among different stakeholders due to its ecological, economic and social impacts (Monceau et al.
2014). However, the social dimension remains understudied and many factors are not taken into consideration (e.g., public perception, stakeholders
knowledge) to increase our understanding of nonnative invasive species dynamics (Larson et al. 2011).
Insufficient consideration of social processes (the
dynamic interactions between individuals, institutions, social organizations and cultural norms) contributes substantially to failure of management
policies (Ban et al. 2013).
In order to analyze ecosystem resilience and/or
resistance in the face of perturbations (e.g., invasive
species introduction) a number of diagnostic
approaches are emerging. In this context, the socialecological system (SES) framework is an interdisciplinary and integrative approach proposed to analyze
and compare SES through a common set of variables
identified in theoretical and empirical research
(Ostrom 2007, 2009; McGinnis and Ostrom 2014).
Ostrom (2009) defined a SES as a complex system
composed of both biophysical and social components
embedded in a network of relationships among them.
The four core subsystems of the focal SES (i.e.,
resource units, resource system, governance system,
and stakeholders) interact to produce outcomes at the
SES level. These subsystems are then decomposed
into second-tier variables, which are further composed
of deeper-level variables that could be used for
delineating the SES. The framework also considers
external variables from related ecological ecosystems
or social-economic-political settings that could affect
the SES (Ostrom 2009). The SES framework is
increasingly used in different countries and disciplines
(e.g., fishery, forestry, freshwater ecosystems, dryland
areas) and still remains in progress (McGinnis and
Ostrom 2014).
The Asian clam Corbicula fluminea (Müller 1774)
is one of the most successful invasive species in
European freshwater environments (Leff et al. 1990;
Sousa et al. 2008a). This species began its worldwide
dispersion at the beginning of the 20th century
associated with human activities such as global trade,
fishing and recreational activities (Counts 1981;
Araujo et al. 1993; McMahon 1999; Darrigran
2002). It colonizes both lotic and lentic habitats (Vidal
A social-ecological system framework to assess biological invasions: Corbicula fluminea…
et al. 2002) and its distribution in invaded rivers ranges
from fresh to brackish waters (Pérez-Quintero 2008;
Sousa et al. 2008b; Vohmann et al. 2010; FerreiraRodrı́guez and Pardo 2014). In addition to its native
range in Asia, the species is currently found in North
and South America, North Africa and in almost all
European river basins (Crespo et al. 2015). C. fluminea
is also included in the Spanish Catalogue of non-native
invasive species (Royal Legislative Decree 630/2013).
Despite the potential threat that C. fluminea represents
to freshwater ecosystems and their biodiversity, the
social and economic factors contributing to its
successful establishment are understudied.
Here we applied the SES framework to understand
the invasion process of C. fluminea in Galicia. To
achieve our objective, we identified and characterized
the following SES subsystems: resource system
(Galician rivers network), resource unit (C. fluminea),
stakeholders (professional and recreational users) and
governance (organizations and rules that govern nonnative species management). Main interactions among
these core subsystems were also characterized to
provide management actions (SES outcomes) for
addressing this biological invasion (Fig. 1). In an
ecological dimension, we aim to test if loss of habitat
quality and native biodiversity provides an empty
niche that can be easily occupied by C. fluminea
resulting in invasions. In social and economic dimensions, since people often recreate in freshwater
systems, we propose that recreational uses linked to
economic development may be important vectors for
C. fluminea dispersal. In addition, we aim to analyze if
increasing social awareness could reduce the rate of
new invaded water bodies. Hence, educational attainment among the population (university or college
studies), and knowledge dissemination through the
mass media were included as explanatory variables.
We also analyze if the implementation of legal
instruments (e.g., specific laws regulating the pet
trade, abolition of border checks and increased
surveillance) would promote or delay C. fluminea
dispersal associated to human activities.
Materials and methods
This study characterized the invasion process of C.
fluminea in the autonomous Community of Galicia
(NW of the Iberian Peninsula, Spain, 29,434 km2)
589
whose population is approximately 2.7 million. Galicia has an extensive hydrographic network; its topography determines the existence of short watercourses
draining to the North into the Cantabrian Sea and
rivers with steep slopes draining to the West into the
Atlantic Ocean. The fishing sector (professional and
recreational users) shapes both the economy and social
identity in Galicia (Gottschalk 1970; Boutureira 1999;
Macho et al. 2013). An integrative approach was used
to map C. fluminea distribution and understand its
dispersal vectors in Galicia. Historical patterns of
distribution and rates of spread (i.e., new records in
invaded waterbodies) were traced with peer-reviewed
publications and non-peer reviewed ‘grey literature’.
In addition, updated distribution data were obtained
with field surveys. Local stakeholder knowledge was
also included to identify dispersal vectors and new
invasions.
We performed a bibliographic search to trace the
distribution of C. fluminea in Galicia by searching
titles, abstracts, and keywords of articles characterizing C. fluminea distribution using the Institute for
Scientific Information (ISI) Web of Science search
engine. We scanned peer-reviewed publications for
different research terms (exotic, invasive species,
Corbicula fluminea, Asian clam, Galicia, freshwater,
river) and their combinations. To carry out the most
thorough literature search possible in the non-peer
reviewed ‘grey literature’ (e.g., personal websites,
technical reports, theses and newspapers) that could
provide relevant information on C. fluminea distribution in Galicia, we searched for similar terms on the
Google.com search engine (Stansfield et al. 2016).
The aim was to gain as much information as
possible to update the C. fluminea distribution map and
to understand its main dispersal vectors in Galicia.
These data were collected from key stakeholders
through semi-structured interviews (n = 20). A semistructured interview is a meeting where open-ended
questions are made by simulating a casual conversation (i.e., without completing a questionnaire) following an interview guide (i.e., general topics to guide the
conversation). Participants were asked about the
distribution and human use of C. fluminea in Galicia
(Online Resource 1). Both, C. fluminea and C.
fluminalis (Müller 1774) occur in Europe, but only
C. fluminea was known to occur in Galicia (Sousa et al.
2007b; Ferreira-Rodrı́guez and Pardo 2016). Hence,
we assumed that all stakeholders referred to the same
123
590
N. Ferreira-Rodrı́guez et al.
Fig. 1 The Galician social-ecological system (SES) for Corbicula fluminea invasion. The four core subsystems of the focal
SES (Resource system, Resource unit, Governance and Stakeholders), their interactions and outcomes, are presented.
Second-tier variables within these subsystems are identified:
resource system (Galician river network), resource units (C.
fluminea), governance (organizations and rules that govern non-
native species management), and stakeholders (fishers, recreational users, local population, NGO’s). Interactions among
variables can be used to identify the most important introduction
vectors and dispersal pathways for C. fluminea. SES outcomes
reveal the capacity of governance to address species introduction, and are related to possible management actions in each
invasion phase. Adapted from McGinnis and Ostrom (2014)
species. Stakeholders were identified at or near our
field survey sites (in the Tambre, Ulla and Miño-Sil
basins). Key stakeholders were local NGO members
and users of the resource system (i.e., divers and
professional and recreational fishers) with extensive
proven knowledge of the area (i.e., visiting the
resource system on a weekly basis). Following
Greenland-Smith et al. (2016), coded responses were
tabulated by the number (n) and percentage (x) of
stakeholders who reported a new location or mentioned C. fluminea use in their interviews.
We included survey data corresponding to fifteen
water bodies in 62 sampling locations. Samples were
collected in spring 2014 adhering to European Water
Framework Directive standards for Spanish invertebrate sampling (Pardo et al. 2014). C. fluminea was
sampled in littoral zones with a kick-net (1 mm mesh
size), and each sample was composed by 20 subsamples (sample area of 0.5 m 9 0.25 m) distributed
proportionally based on the most representative
littoral habitats (e.g., sand, gravel, vegetal detritus),
representing [ 5% of the sampling area in a 100-m
fixed river stretch length (total sampled area for 20
kick samples of 2.5 m2).
To characterize the SES, we identified a quantifiable set of variables based on four primary dimensions
(social, ecological, economic and governance). We
adapted the second-tier variables proposed by Basurto
et al. (2013) with respect to introduction pathways and
dispersal vectors for non-native species. Based on
previous works (Ruiz et al. 1997; Dextrase and
Mandrak 2006), the most common pathways for
non-native species introduction in estuaries and
freshwaters were included as variables (i.e., gross
imports, exotic pet trade, and sport fishing licenses).
Other key variables affecting non-native species
introduction (population of a given country, loss of
native biodiversity, habitat quality, and warming)
were adapted from case studies (see Garcı́a-Berthou
et al. et al. 2005; Dextrase and Mandrak 2006; Rahel
and Olden 2008). Furthermore, increased scientific
knowledge on non-native invasive species in a region
123
A social-ecological system framework to assess biological invasions: Corbicula fluminea…
(represented by the number of peer-review scientific
papers published) was included in our study. Similarly, we have included variables of the education
attainment among the population (number of university students) and non-native invasive species portrayed in mass media (number of news about nonnative invasive species). Following Basurto et al.
(2013), some governance variables remained constant
over time and were therefore not a source of variance
and thus not included in the analysis (e.g., policy area,
geographic range, regime type). On this basis, we
selected a total of 18 second-tier variables nested
within the four core subsystems of the focal SES.
Information on these variables was gathered from
1980 to 2014. The final matrix dimension was
35 years by 18 variables. Detailed information about
these variables is given in Table 1.
We used a principal component analysis (PCA) to
reduce the dimensionality of second-tier variables to
five components. The most explanatory components
explaining 70–80% of the variance were selected
following the Cattell’s scree test (Cattell 1966), which
consists of plotting the eigenvalues (y-axis) against the
components (x-axis), and inspecting the shape of the
resulting curve for a large change in the slope. This
point on the curve indicates the maximum number of
components to retain for the analysis. Pairwise
Spearman’s correlation coefficients were calculated
for all combinations of PC axes scores and the number
of water bodies invaded by C. fluminea in Galicia. In
addition, differences between the number of water
bodies invaded by C. fluminea pre- and post-implementation of legislative instruments (Schengen Agreement and the Spanish Nature Conservation Law on
Natural Heritage and Biodiversity, hereinafter Law
42/2007) were computed and compared using the
Wilcoxon test. SPSS v.15.0 software was used for all
data processing and statistical analyses.
Results
The invasion history of C. fluminea in Galician water
bodies was reconstructed following Sakai et al. (2001).
Before 1920, C. fluminea was confined in its native
range. Then, the species was introduced in North
America in the 1920s and Europe in the 1980s,
surpassing geographical barriers (i.e., Pacific and
Atlantic oceans). In 1989 the species was first recorded
591
in Galicia (River Miño; Araujo et al. 1993) derived
from the River Tagus probably associated to human
activities (e.g., leisure craft, sport fishing, or pet trade).
After a lag phase where the species surpassed the local
environmental barriers the exponential growth phase
started—from 1996 to 2005. In 2005, maximum
population densities were recorded in the River Miño
(up to 4000 ind. m-2). Hereafter, new water bodies
were invaded all over the region (Table 2).
In the last 15 years, our long-term information
gathered from several sources showed new records in
the Centeáns ponds (Ayres 2008), and the Deva
(empty shells), Mero and Sil rivers (Lois 2010).
Additionally, the grey literature signaled its presence
in the Pontiñas stream in 1997 and in the Antela pond
in 2002 (de la Cigoña and Oujo 2002).
While nearly all the stakeholders interviewed
(n = 18, x = 90%) were aware of the presence of C.
fluminea in nearby rivers, only two reported new
locations, with empty shells in the Tambre river in
2009 and in the Tea river in 2013. When discussing C.
fluminea uses, responses indicating no use of this
species (n = 15, x = 75%) were more common than
positive responses (n = 5, x = 25%). The most common use was for food for humans (n = 3, x = 15%),
followed by its use as bait in sport fishing (n = 2,
x = 10%).
Our field sampling data reported the presence of C.
fluminea in 16 of 62 sampled localities (Fig. 2) along
Galician water bodies with a density (mean ± SD) of
544 ± 790 ind. m-2. C. fluminea was found in Miño,
Sil, Ulla and Mero rivers, but not in Tea or Tambre
rivers where it had previously been reported. In
addition, no live or dead individuals were found in
Anllóns, Eume, Eo, Lérez, Louro, Masma, Mandeo,
Sor and Umia rivers. The highest densities were found
in the River Ulla (845 ± 1330 ind. m-2) and in the
River Miño (702 ± 914 ind. m-2). In the River Mero,
C. fluminea density was much lower (360 ± 241
ind. m-2). Low densities were recorded at the limit of
the invaded area in the Miño-Sil basin (River Sil:
5 ± 1 ind. m-2). Detailed information is given in
Online Resource 2.
Spatial data from field surveys together with
historical records from peer-reviewed publications
and non-peer reviewed ‘grey literature’ indicated a
mean upstream spread along the Miño, Ulla and Mero
rivers of 3.6 km yr-1. In the Miño-Sil basin, C.
fluminea reaches 197 km upstream from the river
123
592
N. Ferreira-Rodrı́guez et al.
Table 1 Social, ecological, economic and governance variables of the SES framework for Corbicula fluminea dispersal in Galicia
Dimension
Variable
Description
Justification
Source
of data
Social
Population
General census of population (number of
persons) living in Galicia
Growth of human population and per capita
resource use as the main drivers of global
change by the industrial and agricultural
development
1
Fishing
licenses
Recreational fishing licenses in force and
expedited by the competent authority in
Galicia
Transport and release of non-native aquatic
organisms used for sport fishing activities
4a
Higher
education
level
University students enrolled in any of the
three Galician universities
General and active interest in nature and
knowledge of non-native invasive species
1, 2
Mass media
news
Number of news about non-native invasive
species yearly portrayed in mass media
Public learning about original scientific
research, new records and impact of
invasive species
5
Gross
domestic
product
(GDP)
Millions of euros of all the finished goods
and services
Dispersal of non-native invasive species
facilitated by the development of transport
networks and human mobility
1
Gross imports
Imports of goods and services in millions of
euros
Direct introduction of non-native species as
‘stowaways’
2, 6
Exotic pet
trade
Thousands of individuals imported alive
with commercial objectives (to Spain)
from captive born or wild species
Accidental and/or intentional release from
the pet industry and aquariums
7
Industrial
productivity
index (IPI)
Indicator which reflects the development of
value added in the different branches of
industry
Loss of water quality through industrial
discharges
1, 2
Endangered
freshwater
species
Number of species placed into one of four
categories of conservation concern (Near
Threatened, Vulnerable, Endangered, and
Critically Endangered)
Average annual temperature
Biotic resistance of native species in
freshwaters to limit the invasion of nonnative species (ecosystem resistance)
3, 9
Increment in the number and distribution
range of warm-temperate non-native
freshwater species, and reduced ecological
resistance of native environments to
invasions
10
Scientific
publications
Peer-reviewed publications queried under
search terms freshwater AND Galicia,
river AND Galicia, invasive species AND
Galicia
Increased knowledge of non-native invasive
species and their distribution and
management
11
Dams
Impoundments in Galicia Costa and MiñoSil hydrographic demarcations
Habitat modification and disruption of
upstream river continuity due to transverse
structures altering flow regimes, blocking
fish migration and facilitating non-native
species establishment
4b
Wastewater
treatment
plants
Cumulative number of wastewater treatment
plants that release treated effluent to
adjacent water bodies
Improvement of water quality to achieving
the over-arching objectives set by the
European Water Framework Directive
4b
Livestock
General census of farm animals, with the
exception of poultry; encompasses cattle,
sheep, pigs, goats, horses (mostly in semiferal conditions), and donkeys
Loss of water quality through increased
nutrient loading from animal waste
1, 2
Economic
Ecological
Temperature
123
A social-ecological system framework to assess biological invasions: Corbicula fluminea…
593
Table 1 continued
Dimension
Governance
Variable
Description
Justification
Source
of data
Agricultural
land
Extent of total cultivated land (rainfed and
irrigated) in hectares, with the exception
of forest plantations
Loss of water quality through increased
concentrations of nutrients, pesticides and
sediment loads
1, 2
Surveillance
Cumulative number of environmental
guard corps responsible for the condition
of the environment and natural resources
Increasing environmental vigilance through
the creation of the Nature Protection Service
(SEPRONA, unit of the Spanish Civil
Guard, 1985) and the Environmental guards
(Civil environmental guard crop, 2000)
responsible for nature conservation and
management of the hunting and fishing
industries
4c
Legislative
instruments
Cumulative number of legislative
instruments related to non-native
invasive species introduction and
dispersal
The Schengen Agreement, implemented in
1995, supposed the gradual abolishment of
the internal borders (and controls) between
European countries. National Legislation
Law 42/2007, further developed by Royal
Legislative Decree 630/2013, created the
first Spanish Catalogue of non-native
invasive species and set a preliminary
framework for taking management measures
for controlling and even eradicating nonnative invasive species. Regulation (UE)
1143/2014 on the prevention and
management of the introduction and spread
of invasive non-native species
14
NGOs
NGOs involved in environmental
governance, including local and regional
groups*
Groups dedicated to environmental protection,
sustainable development, surveillance,
invasive species eradication, and other proenvironmental issues
4
Source of data: 1INE (Instituto Nacional de Estadı́stica), 2IGE (Instituto Galego de Estatistica), 3DOGA (Diario Oficial de Galicia)
Decreto 88/2007, 4Xunta de Galicia, aConsellerı́a do Medio Rural, bAugas de Galicia, cServizo de Conservación da Natureza,
5
Autonomic newspaper (Faro de Vigo), 6Tizón (2002), 7CITES, 9IUCN, 10Meteogalicia, weather stations network, 11ISI Web of
Knowledge, 14Boletı́n Oficial del Estado (BOE). *Data corresponding to 82 environmental NGOs from Lugo (one of the four
provinces in the Galician region) have been excluded from the analysis due to their unreliability
mouth, indicating maximum spread rates of
9.2 km yr-1 (Table 3).
The PCA showed that the first two components
explained 76.74% of the variance (Table 4). The first
component (57.91% of total variance) was linked to
variables of the social (higher education level and
mass media news), ecological (endangered freshwater
species, scientific publications, dams, wastewater
treatment plants, livestock, and agricultural lands),
economic (GDP, gross imports, and IPI) and governance (surveillance, legislative instruments, and
NGOs) dimensions. The second component (18.83%
of the variance) made reference to the social (population, sport fishing licenses, and higher education
level), ecologic (livestock) and governance
(legislative instruments) dimensions. Spearman’s correlation between the 2 PC scores and the total number
of water bodies invaded by C. fluminea in Galician
freshwaters showed a positive correlation with PC1
(r = 0.982, P = 0.0001). A non-significant correlation
was found with PC2 (r = - 0.066, P = 0.71).
Our results indicated that the number of new water
bodies invaded by C. fluminea remained stable postimplementation of the legislative instruments (Wilcoxon Z = - 1.604, P = 0.109). No differences were
found in the number of new water bodies invaded by
C. fluminea (Wilcoxon Z = - 1.289, P = 0.197) preand post-implementation of the Schengen Agreement.
123
594
N. Ferreira-Rodrı́guez et al.
Table 2 Conceptualization of the Corbicula fluminea invasion
process in Galicia (NW Iberian Peninsula). The status of C.
fluminea is assessed year-to-year in each invasion stage and
barriers overcome between each one, with special emphasis on
the possible management action in each phase. Source: adapted
from Richardson et al. (2000) and Sakai et al. (2001), own
compilation from interviews and field data
Year
Status
Invasion phase
Management
options
Comments
Before 1980
Native species
Native range
Prevention
Native from the eastern Mediterranean to southwestern Asia;
parts of Africa and Australia. Introduced in North America in
the 1920s and Europe in the 1980s
Transport
Prevention
Transport between Iberian Atlantic basins associated to
commercial fishing gear, leisure craft and use as sport fishing
bait for cyprinids, pet trade and deliberate or accidental
introduction
Establishment
Eradication
The species establishes a self-sustaining population by
surviving environmental conditions and biotic interactions
and successfully reproduce. First record in the Miño river in
1989, derived from a unique introductory event of the species
in the River Tagus (1980)
Lag phase
Eradication
Low population size, evolution and adaptation to the new
habitat characterized by low spread rates. Observed spread
rate: 1.5 km yr-1
Exponential
growth
Control/
Restoration
Expansion phase marked by increasing spread rates and
unregulated exponential growth. Maximum population
densities surpassed 4000 ind. m-2. Population decreases to
2000 ind. m-2 in 2005 summer heatwave (Sousa et al.
2008b). Observed spread rate: 2.9 km yr-1
Dispersal
Control/
Restoration
Population density stabilizes (ca. 3000 ind. m-2; FerreiraRodrı́guez and Pardo 2018). Secondary dispersal resulting
from biological features in conjunction with human activities.
The Centeáns ponds and River Ulla (2008); River Tambre
(2009); Deva, Sil and Mero rivers (2010), River Tea (2013).
Possible records at the Antela pond and Pontiñas stream.
Observed spread rate: 9.2 km yr-1
Geographical barriers
1980–1989
Introduced
species
Environmental (local) barriers
1989
Casual species
Reproductive barriers
1989–1996
Naturalized
species
Reproductive barriers
1996–2005
Invasive species
Barriers to dispersal
2008–the
present
Invasive species
Environmental and biotic barriers (disturbed habitats)
At present
Invasive species
Ecological and
human
impacts
Control/
Restoration
Discussion
The SES framework was a useful tool in identifying
variables related to non-native species in freshwater
environments. Our case study from Galicia supports
the idea that the increasing distribution range of C.
fluminea is closely associated with the social, ecological, economic and governance dimensions of the SES.
123
Changes in sediment biogeochemical composition, negative
effect on native bivalve abundance and diversity, substrata for
invertebrate settlement, facilitation of native and non-native
fauna (Richardson et al. 2000, Sakai et al. 2001; Vander
Zanden and Olden 2008)
Applying the SES framework to C. fluminea invasion
had several strengths: (1) it facilitated the integration
of data from different disciplines (Janssen and
Anderies 2013), including diverse quantitative and
qualitative data; (2) it allowed the explicit consideration of the governance as tool to prevent the
introduction into new waterbodies; and (3) as none
of four multi-linked core subsystems (resource units,
A social-ecological system framework to assess biological invasions: Corbicula fluminea…
Fig. 2 Current known distribution of Corbicula fluminea in
Galicia (NW Iberian Peninsula). Closed circles—C. fluminea
presence, stars—empty shells, diamonds—presence reported in
595
grey literature. Only main tributary rivers are depicted Source:
literature review, own compilation from interviews and field
data (n = 62 sampling locations)
Table 3 Summary of data related to the mean annual upstream spread (km from the river mouth) rate by Corbicula fluminea, either
actively or by means of passive transport with natural or anthropogenic vectors
Basin
River
Year
Miño-Sil
Miño
1989
Ulla
Mero
Years post-invasion
0
Distance (km)
Spread (km yr-1)
Source of data
13
–
Araujo et al. (1993)a
Miño
2004
15
44
2.1
Pintos and Fernández (2004)
Miño
2006
17
76.2
3.7
Lombardero (2006) (Grey literature)
Sil
2009
20
197
9.2
Lois (2010)
Ulla
2008
0
2.8
–
Angueira (2013) (Grey literature)a
Ulla
2014
6
13.9
1.9
Present results
Mero
2009
0
8.6
–
Lois (2010)a
Mero
2014
5
14.3
1.1
Present results
a
Denotes first record in the basin
resource system, governance system and stakeholders)
can be completely understood in isolation, the SES
framework was well-suited to incorporate the complexity of a biological invasion in the analyzed system.
In addition, the SES framework had an explicit focus
on stakeholders in the system. In this regard, our study
highlights the importance of collaborating efforts
between stakeholders and academic institutions for
early detection of new invasions and to develop
management strategies jointly with decision-makers.
Corbicula fluminea invasion
The origin of C. fluminea invasion in Galicia remains
highly uncertain. Recent genetic studies have suggested that C. fluminea in the region resulted from a
123
596
Table 4 Explained
variance of the first two
components and variables
loading in the Principal
Components Analysis of the
social, ecological,
economic, and governance
dimensions analyzed from
1980 to 2014. Highest
variables loadings are
indicated in bold for each
axis
N. Ferreira-Rodrı́guez et al.
Dimension
Social dimension
Ecological dimension
Economic dimension
Governance dimension
unique introduction event of the species in the River
Tagus (Portugal), which subsequently dispersed to
other freshwater ecosystems (Gomes et al. 2016).
Taking the population dynamics of invasive species
into consideration (Sakai et al. 2001), successful
establishment is usually followed by an exponential
growth phase, where the population starts to produce
sufficient number of larvae, and dispersal can drive the
invasive species to colonize new areas (Arim et al.
2006). Assuming that expansion progressed upstream
gradually, our results (mean upstream spread of
3.6 km yr-1) are similar to those previously reported
for other European watercourses (e.g., the Elbe and
Rhine rivers: 2.4 km yr-1; Beran 2006; Schmidlin and
Baur 2006). Despite the existence of great barriers to
dispersal in the Miño river catchment (twenty-three
larger dams; more than 25 m high), we found a
maximum spread rate of 9.2 km yr-1, which may be
related to human activities (e.g., use as fishing bait) or
to aquatic birds (i.e., attached to feet or feathers
through mucous threads secreted by small individuals
of C. fluminea; Prezant and Chalermwat 1984). In fact,
early works have identified flotation as a means of
downstream dispersal in small individuals of C.
fluminea (Yavelow et al. 1979). In contrast, without
human intervention, upstream dispersal in freshwaters
may be slower and limited to crawling of juveniles and
123
Variable
PC#1
PC#2
Population
- 0.250
0.808
Sport fishing licenses
- 0.035
- 0.948
Higher education level
0.602
- 0.754
Mass media news
0.657
0.485
Endangered freshwater species
0.966
0.026
- 0.355
Temperature
0.068
Scientific publications
0.901
0.315
Dams
Wastewater treatment plants
0.984
0.964
- 0.055
0.214
Livestock
- 0.590
- 0.522
Agricultural lands
- 0.894
0.010
Gross domestic product (GDP)
0.976
0.116
Gross imports
0.960
0.179
Exotic pet trade
0.179
- 0.041
Industrial productivity index (IPI)
0.771
- 0.368
Surveillance
0.926
- 0.138
Legislative instruments
0.663
0.533
NGOs
0.988
- 0.035
adults (mean upstream spread of 1.2 km yr-1) and
tidal transport of larvae and floating juveniles during
rising tides in estuaries, especially during spring tides
(Voelz et al. 1998; Rosa et al. 2014).
Social and economic dimensions
Since the beginning of the 21th century, news in mass
media about non-native invasive species greatly
increased. Together with the higher education level
attained by the population, the knowledge dissemination through the mass media should increase public
awareness about the impact of non-native invasive
species. Nevertheless, field results suggest that human
activities seem to be the main drivers of its introduction in new water bodies. This assumption is supported
by the presence of empty shells in the Deva, Tea and
Tambre rivers, probably related with the use of C.
fluminea as bait in sport fishing. Despite the wide
spatial coverage of our surveys, we were unable to find
live individuals in the Tea or Tambre rivers, supporting the idea of human-mediated dispersal. This
concept has been corroborated by personal interviews
and it is reported in grey literature (e.g., Lorenzo
2014), although there is no evidence from our analysis
to support such assumption.
A social-ecological system framework to assess biological invasions: Corbicula fluminea…
The economic dimension (mainly given by the
GDP, gross imports, and IPI variables) suggests that
economic health of the region was associated with the
dispersal of C. fluminea. Indeed, this economic
dimension was previously identified as one of the
main predictors of non-native species richness (Gallardo 2014; Keller et al. 2009). One component in the
increasing globalization of the economy is the biological exchange among distant geographical regions
through international transport and trade. In fact,
countries with the greater degree of international trade
tend to have more non-native invasive species by the
development of terrestrial transport networks, migration rates, number of tourists visiting the country, and
trade commodities (Dalmazzone 2000; Westphal et al.
2008). In addition, current trade agreements are
fostered through relaxing restrictions that may prevent
the introduction of non-native invasive species
(Campbell 2001). Large development projects, such
as dams, irrigation schemes, land reclamation, and
road construction, have also contributed to dispersal of
non-native invasive species (McNeely 2001).
The commercial fishing industry is a key economic
engine in Galicia. There, the River Miño supports an
important traditional fishing community that carries
out its commercial activity using artisanal fishing
methods. Since the 1960s, barriers to fish migration (in
the form of dam construction), loss of water quality
(associated to urban waste, agricultural runoff, and
livestock farms) and overexploitation have resulted in
the extirpation of species of local cultural and
economic importance (e.g., European Atlantic sturgeon Acipenser sturio Linnaeus, 1758) and a decline in
species which depend on the continuity of the river to
complete their life cycle [e.g., Atlantic salmon Salmo
salar (Linnaeus 1758), European eel Anguilla anguilla
(Linnaeus 1758)] (Dill 1993). Since the collapse of
fisheries in the mid-1980s (Online Resource 3), and
encouraged by its occasional consumption, exploitation of C. fluminea stocks has been highlighted as an
effective management action and a new economic
alternative for local fishers (e.g., Lombardero 2006;
Vizoso 2008; Ilarri and Sousa 2012). However, this
strategy may result in unintended environmental
impacts, like deliberate introductions, if it is organized
around economic goals rather than environmental
goals (van Beers and van den Bergh 2001).
597
Ecological dimension
The increasing body of scientific knowledge allowed
the identification of new C. fluminea invaded water
bodies in Galicia. This knowledge was a key factor to
decipher the important role of native biodiversity to
strengthen ecosystem resilience and/or resistance to
environmental fluctuations and disturbances. In this
regard, high biodiversity was signaled as a key
component of ecosystems preventing the establishment of non-native species at high densities (e.g.,
freshwater mussels providing ecosystem resistance to
C. fluminea invasion; Vaughn and Spooner 2006). Our
results are consistent with this observation that native
biodiversity may be negatively related to the increasing area occupied by C. fluminea. Hence, native
species conservation should represent an effective
strategy preventing the establishment of non-native
species at high densities. The benthic community
structure of the freshwater environments of northwestern Iberian Peninsula has been impacted by
human activities for thousands of years (de Agüero
et al. 2014). Nonetheless, the impact upon the benthic
community has clearly become much more intense
since the middle of the 20th century due to hydromorphological alterations (i.e., dam construction), fish
overexploitation and pollution (Dill 1993). These
changes to community structure have left the ecosystems more vulnerable to biological invasions (Manchester and Bullock 2000; Carlsson et al. 2009). One
example is the decline of native freshwater mussel
species such as Unio delphinus Spengler, 1793 and
Margaritifera margaritifera (Linnaeus 1758) (Bauer
1986, 1988; Araujo 2011) that could have competed
with C. fluminea and prevented the establishment of
high density populations. In the last three decades, the
improvement of environmental conditions (e.g.,
derived from the increasing number of wastewater
treatment plants, reduction of agriculture land surface,
and reduction in the livestock), the absence of
potential predators (e.g., extirpation of the European
Atlantic sturgeon; Ferreira-Rodrı́guez et al. 2016) and
the presence of empty niches (e.g., by decline of native
freshwater mussels) might have favored the successful
establishment of C. fluminea.
123
598
N. Ferreira-Rodrı́guez et al.
Governance dimension
Management implications
Our results highlight that increasing surveillance was
positively related with the detection of new C.
fluminea invaded water bodies. Such effectiveness of
environmental guard corps represents a management
opportunity in the implementation of early detection
and eradication programs. Legislative instruments
detailed well-defined measures for non-native invasive species governance and governability. As a result,
rules-in-use (i.e., Law 42/2007 and Royal Legislative
Decree 630/2013) should stop repeated introductions
of enlisted species. Nevertheless, despite the implementation of more restrictive legislative instruments,
new water bodies were invaded in the region year to
year. In recent years, the Galician government has
demonstrated high dynamic resilience, implementing
specific management actions as a rapid response to
non-native invasive species. This is the case of species
able to cause ecological, economic and social impacts
(e.g., the red palm weevil Rhynchophorus ferrugineus
Olivier, 1870, the pine wood nematode Bursaphelenchus xylophilus (Steiner and Buhrer 1934) Nickle
1970 and the eucalyptus weevil Gonipterus scutellatus
Gyllenhal, 1833; for more details on these preventive
and control plans see http://cmaot.xunta.gal/). The
governability dynamics concerning these non-native
invasive species include collaborative efforts among
different stakeholders (authorities, scientists, society
and producers) to achieve ‘primary management’
goals (control and eradication measures). In addition
to government surveillance, our analysis indicated that
the number of environmental NGOs was positively
related with the record of new invaded waterbodies. It
is therefore reasonable to think that the pro-environmental stance and educational mission of NGOs may
strengthen the implementation of management
strategies (Gemmill and Bamidele-Izu 2002).
Although legislative instruments for managing nonnative invasive species have been approved, they are
yet to be successfully implemented. Additionally, two
recent legislative instruments (Royal Legislative
Decree 630/2013, National legislation regulating the
Spanish list of invasive non-native species; Regulation
(EU) 1143/2014, European legislation on invasive
non-native species) have been approved, but insufficient time has elapsed to assess their effectiveness.
Our results suggest that diagnostic application of the
SES framework is useful for understanding the
complexity of biological invasions. Despite increasing
regulatory pressure on non-native invasive species,
governments still often fail to take notice and face the
real dimension of the problem. An innovative aspect
of the SES framework here presented is its utility for
managers to select which of the framework’s variables
will be particularly relevant for avoiding non-native
species introduction and dispersal. We have shown
that legislative instruments alone cannot adequately
avoid such introductions because their implementation is conditioned by the context in which they are
applied; i.e., the socioeconomic development and
environmental characteristics of the system addressed
should be accounted for. In this regard, the SES
framework organizes key variables for the governance
of the SES at multiple hierarchical levels, which is also
useful for identifying key action items for legislative
instruments
addressing
non-native
species
introduction.
In the case of Galicia, the resource system is
characterized by a vast river network that makes the
region particularly susceptible to secondary dispersal
processes of freshwater non-native invasive species
once introduced. Additionally, biological features of
non-native invasive species in conjunction with
human activities may facilitate their introduction into
new water bodies. Our field results suggest that leisure
activities such as sport fishing may be related with C.
fluminea secondary dispersal and should be the focus
of policy prescriptions and environmental education
(preventive) programs.
Since a single individual of C. fluminea can
establish a new population through self-fertilization,
its eradication is impossible in most cases (Vander
Zanden and Olden 2008). Hence, prevention of further
introductions is of primary importance. In this regard,
our study and other previous works (e.g., Szekeres
et al. 2013) highlight the importance of collaborating
efforts between stakeholders (fishers, recreational
users, local populations, environmental guard corps
and NGOs) and academic institutions for early detection of new invasions and to develop management
strategies jointly with decision-makers. As an example, local fishermen in the River Tagus recognized the
presence of C. fluminea and its use as fishing bait in the
123
A social-ecological system framework to assess biological invasions: Corbicula fluminea…
early 1950s (Sousa et al. 2007a), thirty years before the
first scientific record in Europe (Mouthon 1981). This
early detection could have provided an opportunity to
address the invasion before the clam’s dispersal
throughout the Iberian Peninsula. On this subject,
Prince (2003, 2010) highlighted the importance of
onsite fishers as civilian aquatic census takers (‘‘barefoot ecologists’’) that should play a key role in
management action plans. This concept has been
applied in fisheries management worldwide (Macho
et al. 2014), mainly in marine fisheries like the smallscale Galician shellfisheries (Macho et al. 2013), but
also in freshwater basins like in the Amazon (Castello
et al. 2013). The involvement of onsite fishers will
provide a rapid and cost-effective detection of nonnative species using a bottom-up strategy (DehnenSchmutz et al. 2010). The involvement of these and
other stakeholders will enhance the development and
implementation of management plans specifically
designed to address the distinctive characteristics of
local, small-scale environments, especially when
scientific knowledge is limited (Cochrane et al. 2011).
Conclusion
C. fluminea started its worldwide expansion at the
beginning of the 20th century associated to human
activities. Due to the increasing number of invaded
water bodies, identifying the introduction pathways
and dispersal vectors of C. fluminea is a key factor in
guiding preventive management actions. Economic
variables, loss of native biodiversity, habitat alteration, improvement of water quality, scientific and
public knowledge, legislative instruments or governmental and non-governmental surveillance are all
predictive of a water body’s susceptibility to invasion
in the short term. Therefore, governments have
approved legislative instruments aimed at addressing
this and other biological invasions. However, they are
yet to be successfully implemented. In this regard, the
SES framework applied here is a useful tool for future
preventive and control plans regarding non-native
invasive species management. Effective management
actions could include freshwater mussel conservation
programs and increasing surveillance, providing
ecosystem resistance to invasions and mitigating the
introduction of non-native species, respectively. In
addition, the ability of decision-makers involving
599
different stakeholders in the real implementation of
legislative instruments should influence how much we
invest in non-native invasive species management and
its outcome.
Acknowledgements We are particularly thankful to J. Iglesias
for his enthusiastic support during field work. Authors are
grateful to T. B. Parr from the Oklahoma Biological Survey
(University of Oklahoma) for his valuable comments that
improved the manuscript. We thank the reviewers for their
careful reading of our manuscript and their many insightful
comments and suggestions. NF-R was supported by a postdoctoral fellowship from the Government of the Autonomous
Community of Galicia (Xunta de Galicia; Plan I2C 2016-2020,
09.40.561B.444.0).
References
Angueira M (2013) La almeja asiática ‘‘invade’’ el Ulla y la
Estación de O Con alerta de la amenaza para especies
autóctonas. Diario de Arousa. http://www.diariodearousa.
com/. Accessed 8 October 2016
Araujo R (2011) Unio delphinus. IUCN Red List of threatened
species, version 2015.3. http://www.iucnredlist.org/.
Accessed 1 December 2016
Araujo R, Moreno D, Ramos M (1993) The Asiatic clam Corbicula fluminea (Müller, 1774) (Bivalvia: Corbiculidade)
in Europe. Am Malacol Bull 10:29–49
Arim M, Abades SR, Neill PE, Lima M, Marquet PA (2006)
Spread dynamics of invasive species. Proc Natl Acad Sci
Unit States Am 103:374–378. https://doi.org/10.1073/
pnas.0504272102
Ayres C (2008) A new record of Asian clam Corbicula fluminea
(Müller, 1774) in Galicia (Iberian Peninsula)-Ribeiras do
Louro e Gandaras de Budiño wetland. Aquat Invasions
3:439–440. https://doi.org/10.3391/ai.2008.3.4.11
Ban NC, Mills M, Tam J, Hicks CC, Klain S, Stoeckl N, Bottrill
MC, Levine J, Pressey RL, Satterfield T, Chan KMA
(2013) A social-ecological approach to conservation
planning: embedding social considerations. Front Ecol
Environ 11:194–202. https://doi.org/10.1890/110205
Basurto X, Gelcich S, Ostrom E (2013) The social-ecological
system framework as a knowledge classificatory system for
benthic small-scale fisheries. Global Environ Chang
23:1366–1380. https://doi.org/10.1016/j.gloenvcha.2013.
08.001
Bauer G (1986) The status of the freshwater pearl mussel
Margaritifera margaritifera L. in the south of its European
range. Biol Conserv 38:1–9. https://doi.org/10.1016/00063207(86)90015-7
Bauer G (1988) Threats to the freshwater pearl mussel Margaritifera margaritifera L. in Central Europe. Biol Conserv
45:239–253.
https://doi.org/10.1016/00063207(88)90056-0
Beran L (2006) Spreading expansion of Corbicula fluminea
(Mollusca: Bivalvia) in the Czech Republic. Heldia
6:187–192
123
600
Boutureira C (1999) La actividad pesquera en la Galicia de los
ss. IX–XIII, a través de la diplomática medieval y la
toponimia actual. Anu Brigant 22:105–134
Cambray JA (2003) Impact on indigenous species biodiversity
caused by the globalization of alien recreational freshwater
fisheries. Hydrobiologia 500:217–230. https://doi.org/10.
1023/A:1024648719995
Campbell FT (2001) The science of risk assessment for phytosanitary regulation and the impact of changing trade
regulations. Bioscience 51:148–153. https://doi.org/10.
1641/0006-3568(2001)051%5b0148:TSORAF%5d2.0.
CO;2
Carlsson NOL, Sarnelle O, Strayer DL (2009) Native predators
and exotic prey–an acquired taste? Front Ecol Environ
7:525–532. https://doi.org/10.1890/080093
Castello L, McGrath DG, Arantes CC, Almeida OT (2013)
Accounting for heterogeneity in small-scale fisheries
management: the Amazon case. Mar Policy 38:557–565.
https://doi.org/10.1016/j.marpol.2012.09.001
Cattell RB (1966) The Scree test for the number of factors.
Multivar Behav Res 1:245–276. https://doi.org/10.1207/
s15327906mbr0102_10
Cochrane KL, Andrew NL, Parma AM (2011) Primary fisheries
management: a minimum requirement for provision of
sustainable human benefits in small-scale fisheries. Fish
Fish 12:275–288. https://doi.org/10.1111/j.1467-2979.
2010.00392.x
Counts C (1981) Corbicula fluminea (Bivalvia: Sphaeriacea) in
British Columbia. Nautilus 95:12–13
Crespo D, Dolbeth M, Leston S, Sousa R, Pardal MA (2015)
Distribution of Corbicula fluminea in the invaded range: a
geographic approach with notes on species traits variability. Biol Invasions 17:2087–2101. https://doi.org/10.1007/
s10530-015-0862-y
Dalmazzone S (2000) Economic factors affecting vulnerability
to biological invasions. In: Perrings C, Williamson M,
Dalmazzone S (eds) The economics of biological invasions. Edward Elgar, Cheltenham, pp 17–30
Darrigran G (2002) Potential impact of filter-feeding invaders
on temperate inland freshwater environments. Biol Invasions
4:145–156.
https://doi.org/10.1023/A:
1020521811416
de Agüero EGG, Garcı́a VB, Rodrı́guez CF, Prieto NF, Garcı́a
JCÁ (2014) Moluscos dulceacuı́colas en yacimientos
arqueológicos: el registro en la provincia de León (Penı́nsula Ibérica). Archaeofauna 23:51–67
de la Cigoña EF, Oujo JM (2002) Falamos do achado berberecho
oriental Corbicula fluminea (Müller, 1774) na canle e
pozas de Antela (Ourense Meridional), ası́ como no rı́o
Pontiñas, en Lalı́n (Pontevedra). In: de la Cigoña EF, Oujo
JM (eds) Colección natureza galega. Asociación Galega
para a Cultura e a Ecoloxı́a, Vigo, pp 7–11
Dehnen-Schmutz K, Chas-Amil ML, Touza J (2010) Stakeholders’ perceptions of plant invasions in Galicia, Spain.
Asp Appl Biol 104:13–18
Dextrase AJ, Mandrak NE (2006) Impacts of alien invasive
species on freshwater fauna at risk in Canada. Biol Invasions 8:13–24. https://doi.org/10.1007/s10530-005-0232-2
Dill WA (1993) Inland fisheries of Europe. FAO, Rome
EASIN (2018) European Alien Information Network, version
7.1. https://easin.jrc.ec.europa.eu/. Accessed 12 June 2018
123
N. Ferreira-Rodrı́guez et al.
Ferguson R (2000) The effectiveness of Australia’s response to
the black striped mussel incursion in Darwin, Australia. A
report of the marine pest incursion management workshop
(No. 75). Marine and Water Division, Environment Australia, Department of Environment and Heritage, Camberra, p 75
Ferreira-Rodrı́guez N, Pardo I (2014) Abiotic controls on population structure of the invasive Corbicula fluminea
(Müller, 1774) in the River Miño estuary. Fundam Appl
Limnol 184:329–339. https://doi.org/10.1127/1863-9135/
2014/0567
Ferreira-Rodrı́guez N, Pardo I (2016) An experimental approach
to assess Corbicula fluminea (Müller, 1774) resistance to
osmotic stress in estuarine habitats. Estuar Coast Shelf Sci
176:110–116. https://doi.org/10.1016/j.ecss.2016.04.017
Ferreira-Rodrı́guez N, Pardo I (2018) Biocontrol: the response
of native oystercatchers to a non-native clam invasion.
J Avian Biol. https://doi.org/10.1111/jav.01633
Ferreira-Rodriguez N, Gessner J, Pardo I (2016) Assessing the
potential of the European Atlantic sturgeon Acipenser
sturio to control bivalve invasions in Europe. J Fish Biol
89:1459–1465. https://doi.org/10.1111/jfb.13019
Galil BS, Nehring S, Panov VE (2007) Waterways as invasion
highways–impact of climate change and globalization. In:
Nentwig W (ed) Biological invasions. Springer, Berlin,
pp 59–74
Gallardo B (2014) Europe’s top 10 invasive species: relative
importance of climatic, habitat and socio-economic factors. Ethol Ecol Evol 26:130–151. https://doi.org/10.1080/
03949370.2014.896417
Garcı́a-Berthou E, Alcaraz C, Pou-Rovira Q, Zamora L, Coenders G, Feo C (2005) Introduction pathways and establishment rates of invasive aquatic species in Europe. Can J
Fish Aquat Sci 62:453–463. https://doi.org/10.1139/f05017
Gemmill B, Bamidele-Izu A (2002) The role of NGOs and civil
society in global environmental governance. In: Esty DC,
Ivanova MH (eds) Global environmental governance:
options and opportunities. Yale Center for Environmental
Law and Policy, New Haven, pp 77–100
Gomes C, Sousa R, Mendes T, Borges R, Vilares P, Vasconcelos
V, Guilhermino L, Antunes A (2016) Low genetic diversity
and high invasion success of Corbicula fluminea (Bivalvia,
Corbiculidae) (Müller, 1774) in Portugal. PLoS ONE
11:e0158108.
https://doi.org/10.1371/journal.pone.
0158108
Gottschalk JS (1970) Fishery management in Spanish Galicia.
Progress Fish-Cultur 32:123–129. https://doi.org/10.1577/
1548-8640(1970)32%5b123:FMISG%5d2.0.CO;2
Greenland-Smith S, Brazner J, Sherren K (2016) Farmer perceptions of wetlands and waterbodies: using social metrics
as an alternative to ecosystem service valuation. Ecol Econ
126:58–69.
https://doi.org/10.1016/j.ecolecon.2016.04.
002
Gurevitch J, Padilla D (2004) Are invasive species a major cause
of extinctions? Trends Ecol Evol 19:470–474. https://doi.
org/10.1016/j.tree.2004.07.005
Ilarri M, Sousa R (2012) Corbicula fluminea Müller (Asian
clam). In: Francis RA (ed) A handbook of global freshwater invasive species. Earthscan, London, pp 173–183
A social-ecological system framework to assess biological invasions: Corbicula fluminea…
Janssen M, Anderies J (2013) A multi-method approach to study
robustness of social-ecological systems: the case of smallscale irrigation systems. J Inst Econ 9:427–447. https://doi.
org/10.1017/S1744137413000180
Jeschke JM, Strayer DL (2005) Invasion success of vertebrates
in Europe and North America. Proc Natl Acad Sci Unit
States Am 102:7198–7202. https://doi.org/10.1073/pnas.
0501271102
Keller RP, Ermgassen PZ, Aldridge DC (2009) Vectors and
timing of freshwater invasions in Great Britain. Conserv
Biol 23:1526–1534. https://doi.org/10.1111/j.1523-1739.
2009.01249.x
Larson DL, Phillips-Mao L, Quiram G, Sharpe L, Stark R,
Sugita S, Weiler A (2011) A framework for sustainable
invasive species management: environmental, social, and
economic objectives. J Environ Manag 92:14–22. https://
doi.org/10.1016/j.jenvman.2010.08.025
Law 42/2007. Ley 42/2007, de 13 de diciembre, del Patrimonio
Natural y de la Biodiversidad. Boletı́n Oficial del Estado,
Madrid
Leff LG, Burch JL, McArthur JV (1990) Spatial distribution,
seston removal, and potential competitive interactions of
the bivalves Corbicula fluminea and Elliptio complanata in
a coastal plain stream. Freshw Biol 24:409–416. https://
doi.org/10.1111/j.1365-2427.1990.tb00720.x
Leuven RSEW, van der Velde G, Baijens I, Snijders J, van der
Zwart C, Lenders HJR, de bij Vaate A (2009) The river
Rhine: a global highway for dispersal of aquatic invasive
species. Biol Invasions 11:1989–2008. https://doi.org/10.
1007/s10530-009-9491-7
Lois S (2010) New records of Corbicula fluminea (Müller,
1774) in Galicia (Northwest of the Iberian Peninsula):
Mero, Sil and Deva rivers. Aquat Invasions 5:S17–S20.
https://doi.org/10.3391/ai.2010.5.S1.005
Lombardero X (2006) La Xunta estudia comercializar el bivalvo
asiático que invade el Miño. La Voz de Galicia. http://
www.lavozdegalicia.es/. Accessed 8 October 2016
Lorenzo S (2014) A vida nos rı́os galegos. http://www.riosgalegos.com/. Accessed 8 October 2016
Maceda-Veiga A, Monleon-Getino A, Caiola N, Casals F, de
Sosto A (2010) Changes in fish assemblages in catchments
in north-eastern Spain: biodiversity, conservation status
and introduced species. Freshw Biol 55:1734–1746.
https://doi.org/10.1111/j.1365-2427.2010.02407.x
Macho G, Naya I, Freire J, Villasante S, Molares J (2013) The
key role of the barefoot fisheries advisors in the co-managed TURF system of Galicia (NW Spain). Ambio
42:1057–1069. https://doi.org/10.1007/s13280-013-04600
Macho G, Naya I, Freire J, Parma A, Prince J, Orensanz J (2014)
The barefoot ecologists: ‘‘Social catalysts’’ and local providers of scientific/technical support for allowing informed
community-based management. In: Kerezi V, Ivany I (eds)
Proceedings of the 2nd World Small-Scale Fisheries
Congress, Mérida, pp 530–531
Maguire LA (2004) What can decision analysis do for invasive
species management? Risk Anal 24:859–868. https://doi.
org/10.1111/j.0272-4332.2004.00484.x
Manchester SJ, Bullock JM (2000) The impacts of non-native
species on UK biodiversity and the effectiveness of control.
601
J Appl Ecol 37:845–864. https://doi.org/10.1046/j.13652664.2000.00538.x
McGinnis MD, Ostrom E (2014) Social-ecological system
framework: initial changes and continuing challenges. Ecol
Soc 19:30. https://doi.org/10.5751/ES-06387-190230
McMahon R (1999) Invasive characteristics of the freshwater
bivalve Corbicula fluminea. In: Claudi R, Leach J (eds)
Nonindigenous freshwater organisms: vectors, biology and
impact. Lewis Publishers, Boca Raton, pp 315–343
McNeely JA (2001) The great reshuffling: human dimensions of
invasive alien species. IUCN, Gland
Monceau K, Bonnard O, Thiéry D (2014) Vespa velutina: a new
invasive predator of honeybees in Europe. J Pest Sci
87:1–16. https://doi.org/10.1007/s10340-013-0537-3
Mouthon J (1981) Sur la présence en France et au Portugal de
Corbicula (Bivalvia, Corbiculidae) originaire dAsie.
Basteria 45:109–116
Ostrom E (2007) A diagnostic approach for going beyond
panaceas. Proc Natl Acad Sci Unit States Am
104:15181–15187.
https://doi.org/10.1073/pnas.
0702288104
Ostrom E (2009) A general framework for analyzing sustainability of social-ecological systems. Science 325:419–422.
https://doi.org/10.1126/science.1172133
Pardo I, Gómez-Rodrı́guez C, Abraı́n R, Garcı́a-Roselló E,
Reynoldson TB (2014) An invertebrate predictive model
(NORTI) for streams and rivers: sensitivity of the model in
detecting stress gradients. Ecol Indic 45:51–62. https://doi.
org/10.1016/j.ecolind.2014.03.019
Pérez-Quintero JC (2008) Revision of the distribution of Corbicula fluminea (Müller, 1744) in the Iberian Peninsula.
Aquat Invasions 3:355–358. https://doi.org/10.3391/ai.
2008.3.3.13
Pintos XP, Fernández XB (2004) As bioinvasións na Galiza.
A Nosa Terra, Vigo
Prezant RS, Chalermwat K (1984) Flotation of the bivalve
Corbicula fluminea as a means of dispersal. Science
225:1491–1493. https://doi.org/10.1126/science.225.4669.
1491
Prince JD (2003) The barefoot ecologist goes fishing. Fish Fish
4:359–371.
https://doi.org/10.1046/j.1467-2979.2003.
00134.x
Prince JD (2010) Rescaling fisheries assessment and management: a generic approach, access rights, change agents, and
toolboxes. Bull Mar Sci 86:197–219
Rahel FJ, Olden JD (2008) Assessing the effects of climate
change on aquatic invasive species. Conserv Biol
22:521–533.
https://doi.org/10.1111/j.1523-1739.2008.
00950.x
Regulation (EU) 1143/2014 of the European Parliament and of
the Council of 22 October 2014 on the prevention and
management of the introduction and spread of invasive
alien species. European Parliament and Council, Brussels
Richardson DM, Pysek P, Rejmánek M, Barbour MG, Panetta
FD, West CJ (2000) Naturalization and invasion of alien
plants: concepts and definitions. Divers Distrib 6:93–107.
https://doi.org/10.1046/j.1472-4642.2000.00083.x
Rosa IC, Pereira JL, Costa R, Gomes J, Pereira ML, Gonçalves F
(2014) Dispersal of Corbicula fluminea: factors influencing
the invasive clam’s drifting behavior. Ann Limnol-Int J
Lim 50:37–47. https://doi.org/10.1051/limn/2014011
123
602
Royal Legislative Decree 630/2013. Real Decreto 630/2013, de
2 de agosto, por el que se regula el Catálogo español de
especies exóticas invasoras. Boletı́n Oficial del Estado,
Madrid
Ruiz GM, Carlton JT, Grosholz ED, Hines AH (1997) Global
invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent, and consequences. Am
Zool 37:621–632. https://doi.org/10.1093/icb/37.6.621
Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With
KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC,
McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller
SG (2001) The population biology of invasive species.
Annu Rev Ecol Syst 32:305–332. https://doi.org/10.1146/
annurev.ecolsys.32.081501.114037
Schmidlin S, Baur B (2006) Distribution and substrate preference of the invasive clam Corbicula fluminea in the River
Rhine in the region of Basel (Switzerland, Germany,
France). Aquat Sci 69:153–161. https://doi.org/10.1007/
s00027-006-0865-y
Sousa R, Antunes C, Guilhermino L (2007a) Species composition and monthly variation of the molluscan fauna in the
freshwater subtidal area of the River Minho estuary. Estuar
Coast Shelf Sci 75:90–100. https://doi.org/10.1016/j.ecss.
2007.02.020
Sousa R, Freire R, Rufino M, Méndez J, Gaspar M, Antunes C,
Guilhermino L (2007b) Genetic and shell morphological
variability of the invasive bivalve Corbicula fluminea
(Müller, 1774) in two Portuguese estuaries. Estuar Coast
Shelf Sci 74:166–174. https://doi.org/10.1016/j.ecss.2007.
04.011
Sousa R, Antunes C, Guilhermino L (2008a) Ecology of the
invasive Asian clam Corbicula fluminea (Müller, 1774) in
aquatic ecosystems: an overview. Ann Limnol-Int J Lim
44:85–94. https://doi.org/10.1051/limn:2008017
Sousa R, Dias S, Guilhermino L, Antunes C (2008b) Minho
River tidal freshwater wetlands: threats to faunal biodiversity. Aquat Biol 3:237–250. https://doi.org/10.3354/
ab00077
Stansfield C, Dickson K, Bangpan M (2016) Exploring issues in
the conduct of website searching and other online sources
for systematic reviews: how can we be systematic? Syst
Rev 5:191
Szekeres J, Akác A, Csányi B (2013) First record of Pectinatella
magnifica (Leidy 1851) in Hungary. Water Res Manag
3:47–49
Tizón JGS (2000) Una serie larga del comercio exterior de
Galicia: el tráfico por aduanas, 1961 a 2000. In: Iglesias
123
N. Ferreira-Rodrı́guez et al.
EL, Femández JJA (eds) Novos escenarios para a economı́a
galega: actas do II Congreso de Economı́a de Galicia.
Universidade de Santiago de Compostela, Santiago de
Compostela, pp 129–156
van Beers C, van den Bergh JCJM (2001) Perseverance of
perverse subsidies and their impact on trade and environment. Ecol Econ 36:475–486. https://doi.org/10.1016/
S0921-8009(00)00245-7
Vander Zanden MJ, Olden JD (2008) A management framework
for preventing the secondary spread of aquatic invasive
species. Can J Fish Aquat Sci 65:1512–1522. https://doi.
org/10.1139/F08-099
Vaughn CC, Spooner DE (2006) Scale-dependent associations
between native freshwater mussels and invasive Corbicula.
Hydrobiologia 568:331–339. https://doi.org/10.1007/
s10750-006-0210-4
Vidal M-L, Basseres A, Narbonne J-F (2002) Influence of
temperature, pH, oxygenation, water-type and substrate on
biomarker responses in the freshwater clam Corbicula
fluminea (Müller). Comp Biochem Physiol C: Toxicol
Pharmacol 132:93–104. https://doi.org/10.1016/S15320456(02)00051-0
Vizoso S (2008) La almeja asiática invade el Baixo Miño y
amenaza la calidad del agua. El Paı́s. https://elpais.com/.
Accessed 21 December 2017
Voelz NJ, McArthur JV, Rader RB (1998) Upstream mobility of
the Asiatic clam Corbicula fluminea: identifying potential
dispersal agents. J Freshw Ecol 13:39–45. https://doi.org/
10.1080/02705060.1998.9663589
Vohmann A, Borcherding J, Kureck A, Bij de Vaate A, Arndt H,
Weitere M (2010) Strong body mass decrease of the
invasive clam Corbicula fluminea during summer. Biol
Invasions 12:53–64. https://doi.org/10.1007/s10530-0099429-0
Westphal MI, Browne M, MacKinnon K, Noble I (2008) The
link between international trade and the global distribution
of invasive alien species. Biol Invasions 10:391–398.
https://doi.org/10.1007/s10530-007-9138-5
Williams SL, Schroeder SL (2004) Eradication of the invasive
seaweed Caulerpa taxifolia by chlorine bleach. Mar Ecol
Prog Ser 272:69–76. https://doi.org/10.3354/meps272069
Yavelow JM, Edlin-Folz E, Golub L (1979) Flotation of the
bivalve Corbicula fluminea as a means of dispersal. Biochim Biophys Acta 583:95. https://doi.org/10.1126/
science.225.4669.1491