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Non-indigenous species in Portuguese coastal
areas, coastal lagoons, estuaries, and islands
ARTICLE in ESTUARINE COASTAL AND SHELF SCIENCE · APRIL 2015
Impact Factor: 2.25 · DOI: 10.1016/j.ecss.2015.06.019

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Retrieved on: 14 July 2015

Estuarine, Coastal and Shelf Science xxx (2015) 1e13

Contents lists available at ScienceDirect

Estuarine, Coastal and Shelf Science
journal homepage: www.elsevier.com/locate/ecss

Non-indigenous species in Portuguese coastal areas, coastal lagoons,
estuaries and islands
c, d, e

nio Fernandes a, Ana Amorim a, b, Se
rgio P. Avila
Paula Chainho a, *, Anto
,
~o J. Castro i, j, Ana C. Costa c, d, Jose
L. Costa a, k, Teresa Cruz i, j,
~o Canning-Clode f, g, h, Joa
Joa
Stephan Gollasch l, Clarissa Grazziotin-Soares a, Ricardo Melo a, b, Joana Micael c,
nica Sousa n,
Manuela I. Parente c, Jorge Semedo m, Teresa Silva i, Dinah Sobral n, Mo
c
a
a, k
Paulo Torres , Vera Veloso , Maria J. Costa
MARE e Marine and Environmental Sciences Centre, Faculdade de Ci^
encias, Universidade de Lisboa, Campo Grande, 1749-016, Lisboa, Portugal
Departamento de Biologia Vegetal, Faculdade Ci^
encias da Universidade de Lisboa, 1749-016 Lisboa, Portugal
c
~o em Biodiversidade e Recursos Gen
rio Associado, Po
lo dos Açores, University of Azores, 9501-801, Ponta
CIBIO, Centro de Investigaça
eticos, InBIO Laborato
Delgada, Portugal
d
Departamento de Biologia, University of Azores, Campus de Ponta Delgada, Apartado 1422, 9501-801, Ponta Delgada, Açores, Portugal
e
Faculdade de Ci^
encias da Universidade Porto, Rua Campo Alegre 1021/1055, 4169-007, Porto, Portugal
f
~o de Biologia Marinha do Funchal, Cais do Carva
~o 9000-107 Funchal, Madeira, Portugal
MARE e Marine and Environmental Sciences Centre, Estaça
g
Centre of IMAR of the University of the Azores, Department of Oceanography and Fisheries/UAz & LARSyS Associated Laboratory, Rua Prof. Dr Frederico
Machado, 4, PT-9901-862, Horta, Azores, Portugal
h
Smithsonian Environmental Research Center, 647 Contees Wharf Road, Edgewater, MD, 21037, USA
i

rio de Ci^
MARE e Marine and Environmental Sciences Centre, Laborato
encias do Mar, Universidade de Evora,
Avenida Vasco da Gama, Apartado 190, 7521903 Sines, Portugal
j


Department of Biology, School of Sciences and Technology, University of Evora, Evora, Portugal
k
Departamento de Biologia Animal, Faculdade Ci^
encias da Universidade de Lisboa, 1749-016 Lisboa, Portugal
l
GoConsult, Grosse Brunnenstr. 61, D-22763, Hamburg, Germany
m
Portuguese Port and Maritime Transport Institute, Lisbon, Portugal
n
Institute for Nature Conservation and Forests, Lisbon, Portugal
a

b

a r t i c l e i n f o

a b s t r a c t

Article history:
Received 8 October 2014
Received in revised form
16 April 2015
Accepted 14 June 2015
Available online xxx

Trends in abundance, temporal occurrence and spatial distribution of marine and brackish nonindigenous species (NIS) are part of the indicators to assess the compliance of Good Environmental
Status in the European Marine Strategy Framework Directive (EU-MSFD). European-wide regional and
national databases for NIS will be useful for the implementation of the EU-MSFD but there are still spatial
gaps for some regions and taxonomic groups. In 2009, Portugal was among the countries with the lowest
reported numbers of NIS in Europe and a national online database on NIS was not available. This study
provides an updated list of NIS registered in Portuguese coastal and estuarine waters, including mainland
Portugal and the Azores and Madeira archipelagos. A list of 133 NIS was cataloged, most of which
recorded in the last three decades, showing that this area of the North Atlantic is no less prone to introductions than neighboring areas. Most NIS reported in the current inventory are native in the IndoPacific region. Fouling and ballast water are the most likely introduction vectors of NIS in the studied
area but shipping routes connecting to the NIS native regions are rare, indicating that most species are
secondary introductions. The high number of NIS in the Azores and Madeira islands indicates that this
ecosystem type seems to be more susceptible to invasions but these preliminary results might be biased
by a higher number of studies and knowledge on the NIS occurrence on the islands.
© 2015 Elsevier Ltd. All rights reserved.

Keywords:
Alien species
National checklist
EU-MSFD
Introduction vectors
Biofouling
Ballast water

* Corresponding author. MARE e Marine and Environmental Sciences Centre,
^ncias, Universidade de Lisboa, Campo Grande, 1749-016, Lisbon,
Faculdade de Cie
Portugal.
E-mail address: pmchainho@fc.ul.pt (P. Chainho).

1. Introduction
The number of non-indigenous species (NIS) known to occur in
estuaries and coastal areas around the world has increased

http://dx.doi.org/10.1016/j.ecss.2015.06.019
0272-7714/© 2015 Elsevier Ltd. All rights reserved.

Please cite this article in press as: Chainho, P., et al., Non-indigenous species in Portuguese coastal areas, coastal lagoons, estuaries and islands,
Estuarine, Coastal and Shelf Science (2015), http://dx.doi.org/10.1016/j.ecss.2015.06.019

2

P. Chainho et al. / Estuarine, Coastal and Shelf Science xxx (2015) 1e13

significantly in the last decades likely due to globalization of international trade, representing a major threat to marine biodiversity and causing severe negative ecological, economic and social
impacts (Bax et al., 2003). Shipping has been identified as the major
vector of introduction of marine NIS but other human mediated
introductions occur via aquaculture and fisheries, aquarium trade,
recreational boating, construction of canals and floating debris or
other mobile structures (Ruiz et al., 2000). NIS might become
established and subsequently invasive due to some attributes that
make them successful in colonizing new areas, namely environmental tolerance, high genetic variability, short generation time,
early sexual maturity, high reproductive capacity, and a broad diet
(Essink and Dekker, 2002). Habitat characteristics also determine
susceptibly for being invaded, with a higher predominance of invasions in disturbed ecosystems and areas with naturally lower
species richness (Essink and Dekker, 2002). Several policy instruments and regulations were created to address the problem of
NIS introductions requiring the implementation of prevention
measures, mainly through the management of introduction pathways and vectors. In Europe, the European Strategy on Invasive
Alien Species (EC, 2008a) encouraged the development of a panEuropean inventory of NIS and required information about NIS
taxonomy and biology, propagule characteristics, dispersion properties and risk assessment predictions. The European Marine
Strategy Framework Directive (EU-MSFD), published in 2008, requires Member States to take the necessary measures to achieve or
maintain Good Environmental Status in marine ecosystems by
2020 (EC, 2008b). The EU-MSFD descriptors for environmental
status assessment include criteria addressing the abundance and
state of NIS, in particular invasive species and their impacts. These
regulations have triggered the compilation of data on NIS and the
development of research projects funded by the European Commission (Occhipinti-Ambrogi et al., 2011). Several NIS inventories
have been published for European countries in the last decades,
such as the national lists for France (Goulletquer et al., 2002),
Norway (Hopkins, 2002), Great Britain (Minchin and Eno, 2002;
Minchin et al., 2013), Greece (Pancucci-Papadopoulou et al.,
2005), Denmark (Jensen and Knudsen, 2005), the Netherlands
(Wolff, 2005), Germany (Gollasch and Nehring, 2006), Belgium
(Kerckhof et al., 2007), Ireland (Minchin, 2007) and Italy
(Occhipinti-Ambrogi et al., 2011). Similarly to other European
countries, records of NIS in the Portuguese coastal and estuarine
ecosystems have been gradually published after the 20th century,
with only a few of these publications referring to introductions that
occurred before that century such as the introduction of the Pacific
oyster (Crassostrea gigas), associated to the Portuguese maritime
exploration (Edwards, 1976) and the barnacles Balanus trigonus and
Amphibalanus amphitrite, introduced into the Azores islands
(Gruvel, 1920). Although several networks and databases that
include information on NIS have been created recently
(Katsanevakis et al., 2012), Portugal is among countries with the
lowest reported numbers of NIS and no national online database on
NIS exists (Katsanevakis et al., 2013). NIS records for Portugal in
online databases of marine species are only available as results from
the projects DAISIE (Delivering Alien Invasive Species Inventories
for Europe; http://www.europe-aliens.org), EASIN (European Alien
Species Information Network (http://easin.jrc.ec.europa.eu) and
more recently in the NIS database AquaNIS, which was developed
during the project VECTORS (Vectors of Change in Oceans and Seas
Marine Life, Impact on Economic Sectors; http://www.corpi.ku.lt/
databases/index.php/aquanis). For the Azores and Madeira archipelagos a list of NIS was provided by Cardigos et al. (2006) and
more recently by Canning-Clode et al. (2013a), respectively. Additionally, a list of non-indigenous macroalgae species registered at
the Azores archipelago was published by Micael et al. (2014). While

DAISIE indicates the occurrence of less than 50 NIS in Portugal
(Katsanevakis et al., 2013), Cardigos et al. (2006) underlined the low
number of NIS in the Azores islands (33) when compared to other
areas, pointing to the isolation and absence of estuaries as a likely
explanation. Canning-Clode et al. (2013a) recorded 16 NIS in
Madeira, emphasizing that surveys were conducted at a single
recreational marina, which may underestimate the NIS records for
this archipelago.
The major objectives of this publication were (i) to present the
first comprehensive inventory of marine and brackish NIS in
Portugal, including mainland and the Azores and Madeira archipelagos (ii) to determine the population status of each NIS and (iii)
assess the relative importance of invasion vectors in Portugal.
2. Methods
Numerous terms related to biological invasions have been used
inconsistently (e.g. Falk-Petersen et al., 2006) and no uniform terminology has been applied in the increasing number of publications on this subject (e.g. Occhipinti-Ambrogi and Galil, 2004). In
this paper NIS were considered as a species, subspecies or lower
taxa introduced by humans, intentionally or unintentionally,
outside of their natural range (past or present) and outside of their
natural dispersal potential. Species that are not demonstrably
native or introduced because either historical records are unavailable or such species possess natural mechanisms of dispersal that
could account for unexpected distributions were termed cryptogenic species (Carlton, 1996) and were excluded in this overview. A
comprehensive literature review was carried out for NIS records,
including mainland Portugal and the Azores and Madeira archipelagos. Publications in scientific journals as well as ‘‘grey literature’’, such as reports of international working groups and projects,
and personal communications, have been consulted and included
as sources of information. Unpublished reports, academic theses
and records from monitoring programs were reviewed and experts
in particular taxonomic groups and/or regions were consulted for
confirmation of doubtful records. Habitats considered were Portuguese coastal areas, estuaries and coastal lagoons, including both
hard and soft substrates and the water column. The Azores and
Madeira archipelagos were included in the islands ecosystem type
since there are no estuaries and coastal lagoons and the continental
shelf is very short. In this study estuaries were considered to extend
from outer coastlines to the limit of tidal waters, including oligohaline and tidal freshwater reaches. NIS have been grouped by
Phyla (Chlorophyta, Dinophyta, Ochrophyta, Rhodophyta, Porifera,
Cnidaria, Ctenophora, Annelida, Bryozoa, Mollusca, Arthropoda and
Chordata) and care has been taken to homogenize nomenclature.
Taxonomic references were updated according to the World Register of Marine Species (Appeltans et al., 2013) and in the case of
algae according to AlgaeBase (Guiry and Guiry, 2015).
The year of the first record and population status were indicated
for the mainland Portuguese territory and for the Azores and
Madeira islands. NIS populations were considered as not established when only a few live specimens were found at a single
location. Species were assumed to be established when there was
evidence of the occurrence of a self-sustaining population, at least
at a specific location in one of the regions considered (i.e. mainland,
Azores and Madeira). Species of unknown status are those where
available information was not sufficiently detailed to support a
reliable classification of the population status. The most recently
known population status of each NIS was provided, although it
could be different from the time of the first record. Although some
NIS were well established when the first reports were published,
authors were consulted to indicate when collections took place.
The most likely vector(s) of introduction for each NIS was

Please cite this article in press as: Chainho, P., et al., Non-indigenous species in Portuguese coastal areas, coastal lagoons, estuaries and islands,
Estuarine, Coastal and Shelf Science (2015), http://dx.doi.org/10.1016/j.ecss.2015.06.019

P. Chainho et al. / Estuarine, Coastal and Shelf Science xxx (2015) 1e13

assigned to 4 broad categories, namely ballast water, fouling,
aquaculture or unknown, using a suite of information including: (i)
site of first occurrence, (ii) source region, (iii) known invasion history, (iv) relationship with aquaculture, intentional stocking, live
food markets, aquaria or bait stores, (v) life cycle characteristics/
ecological attributes, (vi) fouling ability, (vii) resting stage production, (viii) known specific vector(s) in other invaded locations
and (ix) first records in areas of shipping activity. For NIS introduced by aquaculture activities both intentional and unintentional
introductions were considered. Portuguese records of live species
imports in 2011 were consulted to determine if any NIS reports
might be related to this pathway. Aquaculture permissions were
also consulted to check if the location of aquaculture facilities
overlapped with the occurrence of cultivated NIS in nature. Some
NIS were assigned to multiple vectors of introduction. When the
available information did not support any reasonable indication of
the likely introduction pathway or a large number of transmission
processes might have been involved, vectors of introduction were
designated as unknown.
The native distribution of NIS was classified in broad oceanic
and continental regions. Ocean regions and ecoregions (Spalding
et al., 2007) were considered to assign species to the following
categories: Adriatic Sea, Ponto-Caspian Region, Mediterranean Sea,
Red Sea, North Sea, Tropical Atlantic, Western Atlantic, Eastern
Atlantic, Northeast Atlantic, Southwest Atlantic, East Pacific, West
Pacific, Indo-Pacific, Indian Ocean, Pan-tropical, South Africa and
sub-polar Antarctic. All species for which the native distribution is
unresolved were assigned as unknown.

3. Results
A total of 133 NIS, included in 12 different Phyla, was cataloged
for the Portuguese coastal areas, estuaries, coastal lagoons and
islands (Fig. 1; Table 1). The temporal evolution of new NIS records
increased irregularly, with nearly 60% of first species records listed
during the last three decades (Fig. 2). Only 4% of NIS were registered
before 1900 and 8% before 1950. The temporal trends in first records for mainland Portuguese territory and the islands were very
similar, although the most significant increase in new records for
Madeira islands occurred more recently (Fig. 2).
Most species classified as NIS were macroalgae (32%),

3

arthropods (14%), tunicates (13%), mollusks (11%) and bryozoans
(9%), with the highest number of species being Rhodophyta (25%)
(Fig. 3). All Phyla except Myzozoa, Chlorophyta, Ochrophyta, Porifera and Ctenophora were represented in the three locations
(Fig. 3).
The highest number of NIS was found in island ecosystems
(Fig. 4), with a total of 85 different species recorded, 64 and 39
species listed respectively for the Azores and Madeira archipelagos
(Fig. 1). A total of 68 different NIS were registered at mainland
Portugal. Estuaries and coastal areas have a very similar number of
NIS, while coastal lagoons were the less invaded ecosystems
(Fig. 4).
In the Portuguese mainland, an increase in NIS occurring in
coastal areas was observed towards the south, with the highest
number registered in the Southern coast, namely in the Algarve
region (Fig. 1). In estuaries and coastal lagoons the highest number
of NIS was found in largest systems, namely in the Tagus (27),
Vouga (aka Ria de Aveiro) (12) and Sado (11) estuaries and in the
lagoon (4) and (Fig. 1). Most NIS showed a restricted
Santo Andre
distribution as for the Portuguese mainland territory 47 NIS were
exclusively recorded in comparison to the Azores and Madeira
archipelagos, while the latter had 27 NIS each, only recorded there
(Fig. 5). Arthropods and mollusks were the Phyla with higher
number of exclusive species in mainland Portugal, while most
exclusive NIS in the Madeira and Azores were Bryozoa and Rhodophyta, respectively (Fig. 5).
Most NIS were considered as established in mainland Portuguese coastal areas (65%) and many of these are at least locally
abundant, with some species having a wide distribution range
(Fig. 6). The number of known established NIS is less dominant in
the Azorean islands (20%), with 13 unestablished species and 21 for
which the population status is unknown (Fig. 6) whereas in the
Madeira archipelago nearly half of the NIS are established while for
the other half the population status was considered as unestablished or unknown (Fig. 6).
Most NIS introduced to Portuguese waters originated from the
wider Indo-Pacific region (46%), with some of these with native
distribution limited only to the Indian Ocean or West Pacific Ocean
(Fig. 7). Nevertheless, the occurrence of species native from the
Indo-Pacific region was predominant in Portuguese mainland locations (63%) but not in the Azores (40%) and Madeira (33%)

Fig. 1. Total number of NIS recorded in major estuaries (Minho, Douro, Vouga, Mondego, Tagus, Sado, Mira and Guadiana indicated by circles, from North to South), coastal areas

, indicated by diamonds) of mainland Portugal, and in the Azores and Madeira archipelagos.
(NW, SW and S coast) and coastal lagoons (Obidos
and Santo Andre

Please cite this article in press as: Chainho, P., et al., Non-indigenous species in Portuguese coastal areas, coastal lagoons, estuaries and islands,
Estuarine, Coastal and Shelf Science (2015), http://dx.doi.org/10.1016/j.ecss.2015.06.019

4

P. Chainho et al. / Estuarine, Coastal and Shelf Science xxx (2015) 1e13

Table 1
List of NIS recorded at mainland Portugal (estuaries, coastal area and coastal lagoons) and Azores and Madeira archipelagos. Potential vectors of introduction are indicated in
superscript characters: a Ballast water, b Fouling, c Aquaculture, d Unknown. Locations where species have been observed during this study have the year of first record
underscored. E Established, NE Not Established, U Undetermined. References relative to first records in Mainland, Azores and Madeira are separated by semicolons.
Year of first record

Taxa

Mainland
Dinophyta
Gymnodinium catenatum Graham, 1943
Gymnodinium microreticulatum Bolsch, Negri & Hallegraeff, 1999
Ostreopsis cf. ovata Fukuyo, 1981
Ostreopsis cf. siamensis Schmidt, 1901

1898d
1999d
2011d
2008d

Chlorophyta
Caulerpa webbiana Montagne, 1837
Codium fragile subsp. fragile (Suringar) Hariot, 1889
Ulva pertusa Kjellman, 1897

2005d
2007d

Ochrophyta
Colpomenia peregrina Sauvageau, 1927
Papenfussiella kuromo (Yendo) Inagaki, 1958
Petalonia binghamiae (J. Agardh) K.L.Vinogradova, 1973
Pseudo-nitzschia multistriata (Takano) Takano, 1995
Sargassum muticum (Yendo) Fensholt, 1955
Undaria pinnatifida (Harvey) Suringar, 1873

Azores

Madeira

2002d
1993b

1951d
1990d
1985b
2003d
1989d
2007d

Rhodophyta
Aglaothamnion cordatum (Børgesen) Feldmann-Mazoyer, 1941

2005
e2007b

Population
status

References

E
E
U
U

Estrada, 1995 (Amorim and Dale, 2006)
Amorim et al., 2001
David et al., 2012
Amorim et al., 2010

E
NE; E
NE

Cardigos et al., 2006
Berecibar, 2011; Titley and Neto, 2005
Berecibar, 2011

E
NE
E
U
E
E

Palminha, 1951
Titley et al., 2009
Yoneshigue, 1985
Churro et al., 2009
Rull Lluch et al., 1994
Araújo et al., 2009

NE

Wallenstein, 2011

E
E; U
E
E
E
NE; E
E; U
E; U
E; E: E

, 1970
Ardre
, 1970; Levring, 1974
Ardre
Berecibar, 2011
Berecibar, 2011
Athanasiadis and Tittley, 1994
Berecibar, 2011; Athanasiadis and Titley,
1994
Araújo et al., 2009; Levring, 1974
Palminha, 1958; Castro and Viegas, 1987
Palminha, 1958; Neto, 1989; Levring, 1974

Anotrichium cf. okamurae Baldock, 1976
Anotrichium furcellatum (J. Agardh) Baldock, 1976
Antithamnion amphigeneum A.J.K. Millar, 1990
Antithamnion densum (Surh) M.A. Howe, 1914
Antithamnion diminuatum Wollaston, 1968
Antithamnion pectinatum (Montagne) J.Brauner, 1994

1960d
1960d
2004d
2004d
2008dd

1989d
1994

Antithamnionella spirographidis (Schiffner) E.M. Wollaston, 1968
Antithamnionella ternifolia (J.D.Hooker & Harvey) Lyle, 1922
Asparagopsis armata Harvey, 1855 (gametophytic and tetrasporophytic
phases)
on, 1845
Asparagopsis taxiformis (Delile) Trevisan de Saint-Le
(gametophytic phase)
Bonnemaisonia hamifera Hariot (tetrasporophytic phase), 1891

2007d
1958d
1951d

1987a,b
1989d

2000d

1929d

E; E

^ncio, 2009; Schmidt, 1929
Vice

b

U; E

Berecibar, 2011; Neto, 1989

E

Wallenstein, 2011

E
E
E
NE

Fredericq et al., 1992
Berecibar, 2011
Berecibar, 2011
Wallenstein, 2011

E
E
E
E; E; E
NE

Gain, 1914
Ferreira et al., 2012
Ferreira et al., 2012
rbara and Cremades, 2004;
Ba
Gain, 1914; Ferreira et al., 2012
Wallenstein, 2011

NE

Wallenstein, 2011

NE

Wallenstein, 2011

NE

Wallenstein, 2011

NE

Wallenstein, 2011

E
E; NE

Berecibar, 2011
Araújo et al., 2009; Wallenstein, 2011

NE; U

Wallenstein, 2011; Haroun et al., 2002

NE

Wallenstein, 2011

NE; U
NE

Secilla et al., 2008; Titley and Neto, 1994
Wallenstein, 2011

E; E

et al., 1974
Berecibar, 2011; Ardre

2003
e2008d

Ceramium cingulatum Weber-van Bosse, 1923
Corynomorpha prismatica (J.Agardh) J.Agardh, 1876
Dasya sessilis Yamada, 1928
Gracilaria vermiculophylla (Ohmi) Papenfuss, 1967
Grallatoria reptans M.A. Howe, 1896
Grateloupia
Grateloupia
Grateloupia
Grateloupia

filicina (J.V. Lamouroux) C. Agarh, 1822
imbricata Holmes, 1896
lanceolata (Okamura) Kawaguchi, 1997
turuturu Yamada, 1941

1974d

1989

1974d

2005
e2007d
1990d
1989d
1989d
2005
e2007d
1914c

1997d

Hypnea flagelliformis Greville ex J. Agardh, 1851

1914b

2005b
2006b
2002b

2005
e2007b
2005
e2007d
2005
e2007d
2005
e2007d
2005
e2007d

Laurencia brongniartii J. Agardh, 1841
Laurencia chondrioides Børgesen, 1918
Laurencia obtusa var. dendroidea (J.Agardh) Yamada, 1931
Laurencia majuscula (Harvey) A.H.S. Lucas, 1935
Lomentaria hakodatensis Yendo, 1920
Neosiphonia harveyi (J. Bailey) M.-S. Kim, H.-G. Choi, Guiry & G.W.
Saunders, 2001
Neosiphonia sphaerocarpa (Børgesen) M.-S. Kim & I.K. Lee, 1999

1970b

2008d
2003d

Pterosiphonia pinnulata (Kützing) Maggs and Hommersand, 1993
Scageliopsis patens Wollaston, 1981
Spongoclonium caribaeum (Børgesen) M.J.Wynne, 1981

2006d

Symphyocladia marchantioides (Harvey) Falkenberg, 1897

2003d

2005
e2007b
2005
e2007b
2005
e2007b
1989d
2005
e2007b
1971d

2001b

Please cite this article in press as: Chainho, P., et al., Non-indigenous species in Portuguese coastal areas, coastal lagoons, estuaries and islands,
Estuarine, Coastal and Shelf Science (2015), http://dx.doi.org/10.1016/j.ecss.2015.06.019

P. Chainho et al. / Estuarine, Coastal and Shelf Science xxx (2015) 1e13

5

Table 1 (continued )
Taxa

Year of first record
Mainland

Porifera
Crambe crambe (Schmidt, 1862)
Desmacella meliorata Wiedenmayer, 1977
vi, 1952
Mycale (Carmia) senegalensis Le
Paraleucilla magna (Klautau, Monteiro & Borojevic, 2004)
Cnidaria
Aiptasia diaphana (Rapp, 1829)
Blackfordia virginica Mayer, 1910
Cordylophora caspia (Pallas, 1766)
Ectopleura crocea (Agassiz, 1862)
Gonionemus vertens A. Agassiz, 1862
Kirchenpaueria halecioides (Alder, 1859)
Maeotias marginata (Modeer, 1791)
Tubularia indivisa Linnaeus, 1758

Azores

1979b
2006b

1989b
<1700a,b,c

Bryozoa
Bugula dentata (Lamouroux, 1816)
Bugula neritina (Linnaeus, 1758)
Bugula simplex Hincks, 1886
Bugula stolonifera Ryland, 1960

2004b

1998d

E

Wirtz, 1998

2013b

E
U
E
E
E
U
U; U

Ramalhosa et al., 2014
Raposeiro et al., 2009
Machado & Cancela da Fonseca, 1997
Cancela da Fonseca, 1989
Morton and Britton, 2000
Knight-Jones and Knight-Jones, 1995
Zibrowius and Bianchi, 1981; Knight- Jones
and
Knight- Jones, 1995

E
E
U
E; E

Norman, 1909
Marchini et al., 2007; Tempera et al., 2001
Morton et al., 1998
Morton et al., 1998; Canning-Clode et al.,
2013
Canning-Clode et al., 2013
Canning-Clode et al., 2013
Vaz-Pinto et al., 2013
Canning-Clode et al., 2013
Canning-Clode et al., 2013
Marchini et al., 2007
Souto et al., 2014; Jullien and Calvet, 1903;
Canning-Clode et al., 2013
Amat and Tempera, 2009; Wirtz and
Canning-Clode, 2009

1995b

1989a,b

2000b
1979b

1980a,b
1995b

1909b
2001b
1998b
1998b

2010b

2012b

1888b

2006b

NE
U
U
E
U
E
E; E; E

2009b

2009b

E; E

2010b
2009b
2010b
2006b
2004b
2004b

2010a

Mya arenaria Linnaeus, 1758

1982a

Amphibalanus eburneus (Gould, 1841)

~ a, 1994
Ocan
Moore, 1987
Cancela da Fonseca, 1989
Cornelius, 1992; Wirtz, 1995
Edwards, 1976
Cornelius, 1992
Muha et al., 2012
Cornelius, 1992

a

Mollusca
Bedeva paivae (Crosse, 1864)
Chaetopleura angulata (Spengler, 1797)
Corbicula fluminea (O. F. Müller, 1774)
Crassostrea gigas (Thunberg, 1793)
Hexaplex trunculus (Linnaeus, 1758)
Mercenaria mercenaria (Linnaeus, 1758)

Arthropoda
Acartia (Acanthacartia) tonsa Dana, 1849
Ampelisca heterodactyla Schellenberg, 1925
Amphibalanus amphitrite (Darwin, 1854)

E
E
E
U; U
U
U
U
U

2009d

Zoobotryon verticillatum Della Chiaje, 1828

Mytilus edulis Linnaeus, 1758
cluz, 1851)
Ocenebra inornata (Re
Pinctada imbricata radiata (Leach, 1814)
Pollia dorbignyi (Payraudeau, 1826)
Potamopyrgus antipodarum J.E. Gray, 1843
Ruditapes decussatus (Linnaeus, 1758)
Tonicia atrata (Sowerby, 1840)
€rch, 1853)
Tonna pennata (Mo
Truncatella subcylindrica (Linnaeus, 1758)
Ruditapes philippinarum (Adams and Reeve, 1850)

1994b

1989b

1993
1979a,b

1916a,b,c
1978a
<1700b,c

1919a,b

1994a,b E
E
E
E
1994a,b E; E
NE

E
1965b

1984c

NE
E
U
E
E
E
E
U
E; U
E

1985a
1986d
1982a,b,c

E
U
E; E; E

1999c
1998b
1998d
1978a,b
<1900c
1985a,b,c
1976d

1889a,b
1998b

References

Duran et al., 2004
Boury-Esnault and Lopes, 1985
Canning-Clode et al., 2013
Borges et al., 2010; Canning-Clode et al.,
2013

2002a,b

Annelida
Branchiomma bairdi McIntosh, 1885
Branchiura sowerbyi Beddard, 1892
Desdemona ornata Banse, 1957
Ficopomatus enigmaticus (Fauvel, 1923)
Hydroides elegans (Haswell, 1883)
Laeospira berkeleyana (Rioja, 1942)
Spirorbis marioni Caullery and Mesnil, 1897

Population
status

2004a,b E
U
2010b
U
b
2006
U; E

1984a,b
1983b

Ctenophora
Vallicula multiformis Rankin, 1956

Celleporaria brunnea (Hincks, 1884)
Parasmittina protecta (Thornely, 1905)
Schizoporella cf. unicornis (Johnston in Wood, 1844)
Schizoporella pungens Canu and Bassler, 1928
Scrupocellaria bertholletii (Audouin, 1826)
Tricellaria inopinata Ambrogi, 1985
Watersipora subtorquata (d'Orbigny, 1852)

Madeira

1998a,b
1897d

2005a,b

U

Houart and Abreu, 1994
Hidalgo, 1916
Mouthon, 1981
Edwards, 1976
Nobre, 1930; Houart and Abreu, 1994
Miguel Gaspar, Portuguese Sea and
Atmosphere
Institute, I. P. (IPMA, IP) (com. pers.)
rio Marítimo da Guia,
Carlos Reis, Laborato
University of Lisbon (com. pers.)
Morton, 1967
Afonso, 2011

Avila
et al., 1998
Morton et al., 1998
Cancela da Fonseca, 1991
Morton, 1967
n, 2013
Arias and Anado
Wirtz, 1998
Martins, 1980; Segerts et al., 2009
Ruano and Sobral, 2000
Sobral, 1985
Marques and Bellan-Santini, 1991
Carvalho et al., 2003; Gruvel, 1920;
Wirtz et al., 2006
Southward, 1998
(continued on next page)

Please cite this article in press as: Chainho, P., et al., Non-indigenous species in Portuguese coastal areas, coastal lagoons, estuaries and islands,
Estuarine, Coastal and Shelf Science (2015), http://dx.doi.org/10.1016/j.ecss.2015.06.019

6

P. Chainho et al. / Estuarine, Coastal and Shelf Science xxx (2015) 1e13

Table 1 (continued )
Year of first record

Taxa

Mainland
Artemia franciscana Kellogg, 1906
Austrominius modestus Darwin, 1854

1980a
1956a,b

Balanus trigonus Darwin, 1854
Callinectes sapidus Rathbun, 1896
Caprella scaura Templeton, 1836

2013b
1978a
1985b

Diamysis lagunaris Ariani and Wittmann, 2000
Eriocheir sinensis H. M. Edwards, 1853
Jasus lalandii (H. M. Edwards, 1937)
Ligia oceanica (Linnaeus, 1767)
Limnoria quadripunctata Holthuis, 1949
Penaeus japonicus Spence Bate, 1888
Palaemon macrodactylus Rathbun, 1902
Percnon gibbesi (H. Milne Edwards, 1853)
re, 1789
Perforatus perforatus Bruguie
Rhithropanopeus harrisii (Gould, 1841)

1995a
1988a
1980a

Madeira

1887a,b

1916b
2013

b

2011a,b

1971a,b
1992a,b

Clavelina dellavallei (Zirpolo, 1825)
Clavelina lepadiformis (O.F. Müller, 1776)
Clavelina oblonga Herdman, 1880
Corella eumyota Traustedt, 1882
Distaplia corolla Monniot, 1975
Microcosmus squamiger Michaelsen, 1927

1971b

1971a,b
1971a
2008b,c
2006a,b

1971a
2009a,b

2006a,b

1998b
1971a,b
2006b
2009a,b
2003b

archipelagos (Fig. 8). NIS native from the Mediterranean Sea and
Atlantic Ocean were more frequent in the Azores (13% and 33%,
respectively) and Madeira (21% and 26%, respectively) islands.
Shipping related vectors were the dominating likely vectors of
introduction of NIS in all locations (Fig. 9), with 28% and 57% of the
NIS that might have been introduced by ballast water and fouling,
respectively. The potential vector of introduction could not be

180
160
140
120
100
80
60
40
20
0

2010a,b

U
U
U
E; E; E

1995a,b E
1995b
U; U
U
E
2004b
E; U
2006b
U; U; U

1969b
1971a,b
1971a,b

Molgula plana Monniot C., 1971
Perophora viridis Verrill, 1871
Polyclinum aurantium Milne-Edwards, 1841
Pycnoclavella taureanensis Brunetti, 1991
Pyura tessellata (Forbes, 1848)
Styela canopus (Savigny, 1816)
Styela cf. plicata (Lesueur, 1823)
Styela clava (Herdman, 1882)

E; E; E
E
U
E
E
U
E
NE
U
U
NE
E
E

1978a,b,c

2009b,c
1970d

Population
status

U
2005a,b E; NE

1998a,b
1995b
1985c
2008a
<1931a

Chordata
Alloeocarpa loculosa C. Monniot, 1974
Ascidia interrupta Heller, 1878
Botrylloides violaceus Oka, 1927
Botryllus schlosseri (Pallas, 1766)

U
E
U
E
E
U
U; E
U

References

Amat et al., 2005
Fischer-Piette and Prenant, 1957;
Wirtz et al., 2006
Chainho, 2014; Gruvel, 1920; Pilsbry, 1916
^ncio and Guerra, 1979
Gaude
Marques and Bellan-Santini, 1985;
Ramalhosa and Canning-Clode, 2015
Cunha et al., 1999
~ a and Ferreira, 1996
Cigon
^ncio, 1982
Guerra and Gaude
Morton et al., 1998
Nolting, 1995
Ruano and Sobral, 2000
Chícharo et al., 2009
Nobre, 1931
Torres et al., 2011
^ncio and Guerra, 1979
Gaude
Monniot, 1974
Monniot and Monniot, 1994
Nagar et al., 2010
Saldanha, 1974; Monniot, 1974;
Canning-Clode et al., 2008
Wirtz, 1995
Monniot, 1974; Wirtz, 1995
Monniot, 1974
Nagar et al., 2010
Monniot, 1974; Wirtz, 2006
Turon et al., 2007; Borges et al., 2010;
Turon et al., 2007
Monniot, 1971
Monniot, 1974
Monniot, 1974
Wirtz, 1998
Monniot, 1974
Canning-Clode et al., 2013
Nagar et al., 2010; this work
Davis and Davis, 2005

determined for a considerable number of species (51), including all
microalgae and most macroalgae species (69%). In contrast, only 7%
of the invertebrate species were introduced by unknown vectors.
Aquaculture was the less significant likely vector identified, with
only 13 species associated to this activity (Fig. 9). Of these, only five
species were exclusively linked to this vector, namely the red algae
Grateloupia filicina, the decapod Penaeus japonicus, the gastropod
Ocenebra inornata and the bivalves Ruditapes decussatus (in the

60
Number of species

Number of NIS

Azores

50
40
30
20
10

0

Mainland

Azores

Madeira
Mainland

Fig. 2. Cumulative number of NIS introduced into brackish and marine environments
in Portuguese mainland, Azores and Madeira archipelagos, over 10 year intervals from
<1900 to >2010.

Azores

Madeira

Fig. 3. Number of NIS introduced into brackish and marine environments in mainland
Portugal, the Azores and Madeira archipelagos, allocated by Phylum.

Please cite this article in press as: Chainho, P., et al., Non-indigenous species in Portuguese coastal areas, coastal lagoons, estuaries and islands,
Estuarine, Coastal and Shelf Science (2015), http://dx.doi.org/10.1016/j.ecss.2015.06.019

P. Chainho et al. / Estuarine, Coastal and Shelf Science xxx (2015) 1e13

100

SEAS (68 NIS)

A-C-M (86 NIS)
Number of NIS

90

Number of NIS

80
70
60
50

45
40
35
30
25
20
15
10
5
0

7

Native distribution

40
30
20

0
Coastal area

Coastal lagoon

Estuary

Island

Fig. 4. Total number of non-indigenous species registered in different ecosystem types
in Portugal and per ecoregion sensus Spalding et al. (2007) are also indicated (SEAS e
South European Atlantic Shelf; A-C-M e Azores-Canaries-Madeira).

Number of species

25
20
15

Fig. 7. Number of marine and brackish water NIS with different native distribution
areas recorded in Portugal.

100%
Number of NIS

10

80%
60%
40%
20%
0%
Mainland

10

Mediterranean Sea

5

Atlantic

Azores

Pacific

Indo-Pacific

Madeira

Indic

Others

Unknown

Fig. 8. Relative number of marine and brackish water NIS with different native distribution areas recorded in mainland Portugal, Azores and Madeira archipelagos.

0

Mainland

Azores

(Treadwell, 1936)] were imported for live bait trade and all others
were aquarium trade species.

Madeira

Fig. 5. Number of marine and brackish water non-indigenous species included in
different taxonomic groups that were registered exclusively within mainland Portugal,
Azores and Madeira archipelagos, allocated by Phylum.

4. Discussion
4.1. Less invaded or less known?

Azores) and Ruditapes philippinarum. The ascidian Corella eumyota,
the cnidarian Gonionemus vertens, the mollusks Chaetopleura
angulata, Crassostrea gigas and Tonicia atrata, and the decapod
Rhithropanopeus harrisii could also have been introduced by aquaculture, although other possible vectors were identified as more
likely for these species. Import permits for bait and aquarium trade
revealed that 125 brackish and marine species were imported to
Portugal, including two species of Porifera, 39 Cnidaria, 36 Annelida, 23 Mollusca, 21 Echinodermata and 4 Chordata. Only two
annelids [Glycera dibranchiata Ehlers, 1868 and Perinereis linea

Population status

70

Number of species

60
50

40
30
20
10
0
Mainland

Unknown

Azores

Not Established

Madeira

Established

Fig. 6. Number of marine and brackish water NIS established, not established and with
unknown population status at mainland Portugal, Azores and Madeira archipelagos.

The introduction of NIS is a worldwide environmental issue
since it represents one of the most important drivers of biodiversity
change (Hulme et al., 2009). Coastal and estuarine ecosystems are
particularly vulnerable to NIS introductions as they are under
permanent exposure to several introduction vectors, such as ballast
water discharge, fouling and aquaculture. NIS databases are
increasingly being used for research (Olenin et al., 2014) but the
state of knowledge of marine biota is still biased by differences on
the availability of basic information, such as NIS national checklists.
All previous databases indicated the occurrence of less than 50 NIS
in Portugal but this study has significantly increased the number of
NIS records in Portugal (133), similar to other recent revisions in
European countries (e.g. Gollasch and Nehring, 2006; Kerckhof
et al., 2007; Occhipinti-Ambrogi et al., 2011; Minchin et al., 2013).
Only Cardigos et al. (2006) and Canning-Clode et al. (2013a) had
published NIS inventories for the Portuguese island habitats but the
current study updated those lists from 33 to 64 species in the
Azores (including the macroalgae NIS reported by Micael et al.,
2014) and from 16 to 39 in Madeira. As emphasized by
Katsanevakis et al. (2013), European countries with a low reported
number of NIS like Portugal did not have a national online database
on NIS. These authors also indicate several factors that might influence the distribution of NIS per country such as (i) the varying
impact of specific pathways of introduction, (ii) the number of
different ecoregions within the country, (iii) the length of coastline
and (iv) the variability in the monitoring and reporting effort. In
spite of the considerable increase in the number of NIS in Portugal it
is almost certainly underestimated. The coastal line is 1860 km

Please cite this article in press as: Chainho, P., et al., Non-indigenous species in Portuguese coastal areas, coastal lagoons, estuaries and islands,
Estuarine, Coastal and Shelf Science (2015), http://dx.doi.org/10.1016/j.ecss.2015.06.019

8

P. Chainho et al. / Estuarine, Coastal and Shelf Science xxx (2015) 1e13

100

Introduction vectors

Number of species

90
80
70
60
50
40
30
20
10
0
Ballast water

Fouling

Mainland

Azores

Aquaculture

Unknown

Madeira

Fig. 9. Most likely vectors of introduction of marine and brackish water NIS in
mainland Portugal, Azores and Madeira archipelagos.

long, including two different ecoregions of the Lusitanian province
(Spalding et al., 2007), namely the South European Atlantic Shelf
(Mainland) and the Azores-Canaries-Madeira ecoregions, which
includes the Azores and Madeira islands. In Portugal there has been
limited historical focus on bioinvasions within the marine and
estuarine environments and most studies were ecological assessments of conspicuous invadors, such as the Chinese mitten crab
Eriocheir sinensis (Cabral and Costa, 1999), the bryozoan Zoobotryon
verticillatum (Amat and Tempera, 2009), the wireweed Sargassum
muticum (Vaz-Pinto et al., 2014) or the Asian clam Corbicula fluminea (Sousa et al., 2009). Some of the earliest records of NIS were
associated with scientific campaigns conducted on specific taxonomic groups, such as Prince of Monaco campaigns for cirripeds,
which included the Azores islands (Gruvel, 1920). The Azores and
Madeira archipelagos were included in several surveys on specific
taxonomic groups such as macroalgae (Gain, 1914; Schmidt, 1929;

Avila,
1998; Wallenstein, 2011; in the Azores; Levring, 1974 in

Madeira), mollusks (Watson, 1897 in Madeira; Morton, 1967; Avila
et al., 1998, 2000; Martins et al., 2009; in the Azores), hydroids
(Cornelius, 1992 in the Azores) and ascidians (Monniot, 1974 in the
Azores). Some broad national surveys were also carried out in the
mainland Portuguese coastal area, on macroalgae (Palminha, 1951,
, 1970; Berecibar, 2011) and cirripeds (Fisher-Piette and
1958; Ardre
Prenant, 1957). The date of first record is therefore mainly related to
the expertise of the early taxonomists working within the region
and thus an unquantifiable bias is associated to those dates and
many of the species listed could have arrived much earlier than the
first record date. This is well illustrated with the invasion pathway
of the dinoflagellate Gymnodinium catenatum in W Iberian waters.
The estimated time of appearance (1889 ± 10), based on the subfossil cyst record, is more than 75 years earlier than the first record
of the species in Iberian waters (1976) (Ribeiro et al. 2012).
Considering that Portugal has some of the oldest shipping routes, a
well-documented vector of marine bioinvasions, it is nearly certain
that marine introductions consistently took place over the centuries of Portuguese colonial history but no formal research focused
on the introduced marine fauna and flora extends to those early
periods. The earliest records of NIS are the importations of the
Pacific oyster from Japan in the 16th century and the unintentional
associated introductions of other species, such as the cnidarian
Gonionemus vertens (Edwards, 1976). The continued increase in the
number of records of NIS and the particularly high number of
newcomers found in the last three decades follows trends identified for other European countries (e.g. Gollasch and Nehring, 2006).
This temporal evolution reflects not only a significant growth of
international trade by shipping, but also a stronger research effort

on biogeography and taxonomic information (Galil, 2008;
Occhipinti-Ambrogi et al., 2011; Minchin et al., 2013), particularly
based on the use of molecular tools. The exclusion of species
considered as cryptogenic also justifies the lower number of NIS in
Portugal when compared to other neighboring countries. Micael
et al. (2014) recently identified 40 species in the Azores islands,
which were classified as cryptogenic and therefore may in future
increase the number of NIS in that archipelago. The amphipod
Corophium orientale Schellenberg, 1928 and the polychaete Cossura
coasta Kitamori, 1960 are good examples of species not included in
the NIS inventory because its occurrence in mainland Portugal is
likely to result from natural expansion of the species distribution. C.
coasta was assigned as a NIS in the Mediterranean (Streftaris et al.,
2005), although it had been previously indicated that it was misidentified in Greece (Read, 2000). The occurrence of this species in
the Mira (unpublished data) and Tagus estuaries (Chainho et al.,
2008) suggests its natural range expansion towards North since
this species is native from southern latitudes, although with no
clearly known origin (Read, 2000). The same range expansion
northward seems to occur for C. orientale, indicated as native from
the Mediterranean, but found more recently in the Guadalquivir
estuary (Cuesta et al., 1996) and present only in southern Portuguese estuaries, such as Ria de Alvor (Rodrigues and Dauvin, 1987),
^ncio
Mira estuary (Chainho et al., 2008) and Tagus estuary (Gaude
and Cabral, 2007). Contrastingly, Gymnodinium catenatum has
been considered an invasive species in the NE Atlantic in all NIS
databases and Amorim and Dale (2006) dated the first occurrence
of the species in the Tagus prodelta (off Lisbon) in 1898 and suggested that it could have been introduced by transport of viable
cysts in ballast tanks. Although the introduction of G. catenatum in
the Lisbon area via shipping cannot be excluded as a possible route,
recent research on cyst records along a latitudinal gradient suggests
a northward natural range expansion from NW Africa (Ribeiro et al.,
2012). Those authors recommended that although G. catenatum can
be considered an invasive species in the NE Atlantic, it should be
included in the list of cryptogenic species.
4.2. Who and where?
Two new/spreading NIS were reported recently, namely the
bryozoan Watersipora subtorquata for the Azores islands and
mainland Portugal and the cirriped B. trigonus for mainland
Portugal. W. subtorquata is a fouling invasive species which has
been widely reported in harbor areas from tropical to temperate
regions (Ryland et al., 2009). It has been found consistently in high
abundances in several different recreational marinas of Lisbon,
Sines and Ponta Delgada (Azores) since 2009 and in several marinas
at the Madeira islands (Canning-Clode et al., 2013b) but its
dispersion to rockyshore natural areas has not been confirmed yet.
The bryozoan Watersipora souleorum (Vieira et al., 2014) was
recently described based on specimens collected in the Atlantic
(Azores, Cape Verde and Senegal), Mediterranean (Naples) and
Indian Ocean (Sri Lanka and India). Additional genetic studies will
be needed to clarify any possible misidentification of Watersipora
specimens registered in Azores, Madeira and mainland Portugal
since specimens from the Azores used in the study of Vieira et al.
(2014) were collected in 1888 (Jullien and Calvet, 1903) and W.
subtorquata and W. souleorum show very similar morphological and
morphometric characters. The occurrence of the cirriped B. trigonus
was known in the Azores and Madeira archipelagos for more than a
century (Gruvel, 1920 and Pilsbry, 1916; respectively) but it had
never been recorded in mainland Portugal until 2013. An established population was observed in a recreational marina located at
the Sado estuary and further research is needed to confirm the
possible occurrence at other locations.

Please cite this article in press as: Chainho, P., et al., Non-indigenous species in Portuguese coastal areas, coastal lagoons, estuaries and islands,
Estuarine, Coastal and Shelf Science (2015), http://dx.doi.org/10.1016/j.ecss.2015.06.019


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