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BioInvasions Records (2019) Volume 8 Article in press
Morais et al. (2019), BioInvasions Records (in press)1
CORRECTED PROOF
Rapid Communication
The Atlantic blue crab Callinectes sapidus Rathbun, 1896 expands its
non-native distribution into the Ria Formosa lagoon and the Guadiana
estuary (SW-Iberian Peninsula, Europe)
Pedro Morais1, Miguel Gaspar2,3, Erwan Garel4, Vânia Baptista2, Joana Cruz2, Inês Cerveira2, Francisco Leitão2
and Maria Alexandra Teodósio2,*
1Department of Environmental Science, Policy, and Management, University of California, Berkeley, Mulford Hall, Berkeley, CA 94720, USA
2Centre of Marine Sciences (CCMAR) University of Algarve, Campus de Gambelas, 8005-139 Faro, Portugal
3Portuguese Institute for the Ocean and Atmosphere (IPMA, I.P.), Avenida 5 de Outubro s/n, 8700-305 Olhão, Portugal
4Centre for Marine and Environmental Research (CIMA), University of Algarve, Campus de Gambelas, 8005-139 Faro, Portugal
Author e-mails: pmorais@ualg.pt (PM), mbgaspar@ipma.pt (MG), egarel@ualg.pt (EG), vania_bap@hotmail.com (VB),
ines.m.cerveira@gmail.com (IC), joanacruz23@hotmail.com (JC), fleitao@ualg.pt (FL), mchichar@ualg.pt (MAT)
*Corresponding author
Abstract
The Atlantic blue crab Callinectes sapidus Rathbun, 1896 is native in the western
Atlantic, however it is a non-indigenous species across Europe since 1900, among
other world regions. In this paper, we report the first occurrences of this species in
the Ria Formosa lagoon and in the Guadiana estuary (SW-Iberian Peninsula,
Europe) which occurred in 2016 and July 2017, respectively. We hypothesize that
the introduction of this species into these ecosystems might be due to the expansion
of the Guadalquivir estuary population through natural processes (larval advection,
active movement), or due to unintended introduction events after being transported
aboard fishing boats, or, less likely, through ballast water. Changes in Guadiana’s
river flow after the construction of the Alqueva dam might also explain the
presence of another non-indigenous species in the Guadiana estuary. The hypotheses
presented, regarding the introduction of the Atlantic blue crab into these ecosystems
and of its co-occurrence with other decapod species, are framed in a broader
context to serve as a future research framework. The use of the Atlantic blue crab
as a new fishing resource is also proposed, namely if it is to be used exclusively by
local communities and if no deleterious impacts upon other fisheries and the
ecosystem occur from this new fishery.
Key words: non-indigenous species, Decapoda, coastal lagoon, estuary, river flow,
dam, fishery
Introduction
The introduction and establishment of non-indigenous aquatic species
results from a series of interconnected mechanisms such as the
characteristics of the introduction vector (Carlton 2011), propagule
pressure (Blossey 2011), and several auto-ecological traits that non-
indigenous species encounter in non-native areas (e.g., abiotic and biotic
resistance) (Hollebone and Hay 2007; Papacostas et al. 2017).
Citation: Morais P, Gaspar M, Garel E,
Baptista V, Cruz J, Cerveira I, Leitão F,
Teodósio MA (2019) The Atlantic blue
crab Callinectes sapidus Rathbun, 1896
expands its non-native distribution into the
Ria Formosa lagoon and the Guadiana
estuary (SW-Iberian Peninsula, Europe).
BioInvasions Records 8 (in press)
Received: 11 December 2017
Accepted: 9 October 2018
Published: 28 January 2019
Thematic editor: Cynthia McKenzie
Copyright: © Morais et al.
This an open access article published under terms
of the Creative Commons Attribution License
(Attribution 4.0 International - CC BY 4.0).
OPEN ACCESS.
New records of the Atlantic blue crab in the Iberian Peninsula
Morais et al. (2019), BioInvasions Records (in press)2
The Atlantic blue crab Callinectes sapidus Rathbun, 1896 (Decapoda,
Brachyura) is a euryhaline species that colonizes marine and estuarine
habitats and is one of many non-indigenous species found in European
waters (Cabal et al. 2006; Castejón and Guerao 2013; Ribeiro and
Veríssimo 2014). The Atlantic blue crab has the potential to impact benthic
communities at multiple trophic levels and displaying significant spatial
and temporal variability between populations (Mancinelli et al. 2013,
2017c). This species is native to the western Atlantic, and its distribution
ranges from Cape Cod (USA) to northern Argentina, including the Gulf of
Mexico (Nehring 2011). Apparently, the Atlantic blue crab is expanding its
distribution north of Cape Cod probably due to warming coastal waters
(Johnson 2015). This species has been observed away from the native range
in Africa, Asia, and Europe (Nehring 2011). Some of these introductions
result from deliberate releases or to multiple independent ballast water
introductions, which is considered the most likely introduction vector
(Nehring 2011). Secondary dispersal from the site of introduction is also
possible (Nehring 2011). Atlantic blue crab was first observed in Europe in
1900 at Rochefort (Atlantic coast of France; Bouvier 1901 in Nehring
2011). Since then, a few viable populations have been established despite
their broad distribution – see Nehring (2011) and Mancinelli et al. (2017a)
for a thorough description of the Atlantic blue crab distribution in its non-
native range. Atlantic blue crab has been reported in areas comprising the
northern and southeastern shores of the Mediterranean sea and adjacent
seas (Adriatic, Aegean, and Black seas) (Mancinelli et al. 2017a), as well as
in the European Atlantic coast – from the Guadalquivir estuary at the Gulf
of Cadiz and further north up to the North Sea and Baltic Sea (Nehring
2011; Mancinelli et al. 2017a). In some of these areas, the species has
established populations (Mancinelli et al. 2017a).
In the case of the Iberian Peninsula (SW-Europe), the Atlantic blue crab
was observed for the first time in its Atlantic coast in 1978 in the Tagus
estuary (western Portugal) (Gaudêncio and Guerra 1979 in Ribeiro and
Veríssimo 2014). This species is also present in the Guadalquivir estuary
(southwest Spain) at least since 2002 (WWF/ADENA 2002 in Castejón and
Guerao 2013). In the Gijon coast, a single specimen was captured in 2004
(Cabal et al. 2006). Another presence record was reported for the Sado
estuary in 2009; however anecdotal accounts suggest for the presence of
this species at least since the mid-1990’s (Ribeiro and Veríssimo 2014). In
the Mediterranean coast of the Iberian Peninsula, the Atlantic blue crab
was found in several sites along the coast of the Balearic Sea (circa
Barcelona and Valencia) and circa Torrevieja (Mancinelli et al. 2017a).
Two new records of the Atlantic blue crab were reported to us by
fishermen describing specimens collected in the Ria Formosa lagoon and
in the Guadiana estuary (southwestern Iberian Peninsula, Europe). Thus,
New records of the Atlantic blue crab in the Iberian Peninsula
Morais et al. (2019), BioInvasions Records (in press)3
Figure 1. Location of the Ria Formosa lagoon (B) and of the Guadiana estuary (C) within the
Iberian Peninsula (SW-Europe) (A). The sites where Atlantic blue crab Callinectes sapidus
Rathbun, 1896 specimens were collected are marked with white dots. In the Guadiana estuary,
the black starts represent the sampling stations (S) where temperature and salinity data was
measured during neap and spring tides. Images retrieved from Google Earth.
this study aims to describe the first report of the Atlantic blue crab in these
ecosystems and to present hypotheses about its introduction. Finally, the
hypotheses laid in the discussion of this paper may serve as a research
framework delving on the invasion ecology of this new non-indigenous
species in the SW-Iberian Peninsula.
Materials and methods
Study areas
The Ria Formosa is a mesotidal coastal lagoon separated from the Atlantic
Ocean by a system of sand barrier islands and inlets (Figure 1B). The
lagoon extends for 55 km along the southern Portuguese coast and has a
maximum width of 6 km. The average depth is 3 m, the tidal amplitude
varies from 1.3 m to 3.5 m, and the lagoon occupies an area of 84 km2 at
the high spring tide (Andrade 1990).
The Guadiana River estuary is a mesotidal estuary with an average depth
of 6.5 m, occupying an area of 22 km2, and the tidal amplitudes range from
1.3 to 3.5 m. The estuary drains into the Gulf of Cadiz (Atlantic Ocean),
extends inland for 70 km, and the last 50 km serve as the southern border
of Portugal and Spain (Iberian Peninsula, Europe; Figure 1C). The Guadiana
River flow varies substantially within and among years due to variation in
rainfall. However, after the completion of the Alqueva dam in February
2002, the river discharge is usually lower than 20 m3 s-1 (Garel and Ferreira
2011), despite episodic flooding events (e.g., March–April 2013).
New records of the Atlantic blue crab in the Iberian Peninsula
Morais et al. (2019), BioInvasions Records (in press)4
Figure 2. Atlantic blue crab Callinectes sapidus Rathbun, 1896 specimen
collected in the Guadiana estuary (SW-Iberian Peninsula, Europe) in July 2017.
Photograph by Vânia Baptista.
Capture and identification of Atlantic blue crab
The Atlantic blue crab specimens collected in the Ria Formosa lagoon and
in the Guadiana estuary were identified according to Williams (1984)
(Figure 2). The total carapace width (± 0.1 cm), fresh weight (± 1 g), and
sex were determined for some of the individuals captured by local
fishermen since they kept most specimens for them. The Atlantic blue crab
was a bycatch in both ecosystems and collected with trammel nets and
traps (Supplementary material Table S1).
Abiotic characterization of the sampling sites
The water temperature and salinity were measured in the Guadiana estuary
in the area colonized by the Atlantic blue crab, using a CTD (Valeport
mini-CTD) recording at 8 Hz and logging data every 0.25 m along the
water column. Two surveys were conducted, one at neap tide (August 31,
2017, tidal range 1.1 m) and one at spring tide (September 8, 2017, tidal
range 3 m). Data were collected at high water slack (i.e., about one hour
after high water level) at four stations (Figure 1C). There is no such data
available for the Ria Formosa lagoon.
Results
The first know accounts of the Atlantic blue crab in the Ria Formosa date
back to 2016 and the first georeferenced capture site is located at 4 km from
the coast (Table S1; Figure 1B). In the Guadiana estuary the first specimen
was collected on July 1st, 2017, at Laranjeiras (Figure 1C; Table S1). As far
as we are aware, the Atlantic blue crab occupies at least a 25-km stretch
along the Guadiana estuary, from the low estuary at Vila Real de Santo
New records of the Atlantic blue crab in the Iberian Peninsula
Morais et al. (2019), BioInvasions Records (in press)5
António and up to the lower upper estuary at Laranjeiras, located at 3 and
28 km away from the coast, respectively (Figure 1C). At least 11 Atlantic
blue crab specimens were collected in the Ria Formosa lagoon, but we only
have detailed information on one specimen (Table S1). However, in the
Guadiana estuary the number of specimens reported to us is bigger and it
ranged from 50 to 60 individuals (Table S1). In the Guadiana estuary, local
fishermen collected 21 males and 5 females (the remaining were not
sexed), the carapace width size ranged from 9.5 cm to 43.4 cm, and the
total fresh weight varied between 65 g and 745 g (Table S1).
In the Guadiana, water stratification was weak during late summer,
being slightly stronger at neap than at spring tides. Water temperature
varied between 24.9 C and 26.1 C, and salinity varied between 14.4 and
27.6 at neap tide, and between 18.3 and 32.4 at spring tide (Table S2).
Discussion
The Atlantic blue crab in the Ria Formosa lagoon and in the Guadiana
estuary
The Atlantic blue crab is one of two non-indigenous Callinectes species
present in Europe (Mancinelli et al. 2017a), the other is rugose swimming
crab Callinectes exasperatus (Gerstaecker, 1856) (Decapoda, Brachyura) – a
single specimen was collected in the Bay of Cadiz (Cuesta et al. 2015).
The Atlantic blue crab has been reported from six sites/regions of the
Iberian Peninsula. The Guadalquivir estuary is the closest site to the
Guadiana estuary and to the Ria Formosa lagoon, which is located 120 km
and 133 km away, respectively. So, four hypotheses may explain the
presence of this species in these ecosystems. First, it might result from the
dispersion of larvae from adjacent colonized ecosystems, as the
Guadalquivir estuary. This hypothesis is supported by the occurrence of a
westwards regional coastal current during ~ 40% of the time around the
year (Garel et al. 2016). Second, adult individuals could have migrated
westwards from the Guadalquivir estuary (Castejón and Guerao 2013),
since this species can perform long-distance migrations (Hill et al. 1989).
Third, the introduction could be due to the transport of live specimens in
the fishing nets of boats coming from colonized ecosystems (e.g.,
Guadalquivir and/or Sado estuaries). Fourth, the colonization of the Ria
Formosa lagoon and of the Guadiana estuary could represent another
independent introduction of this species into European coastal waters via
ballast water, however there is no transoceanic shipping in these sites.
Therefore, the origin of these blue crab populations is uncertain and only a
comprehensive genetic study can shed light on this matter. This genetic
approach is essential for a future research framework on the Atlantic blue
crab in these two ecosystems.
New records of the Atlantic blue crab in the Iberian Peninsula
Morais et al. (2019), BioInvasions Records (in press)6
Changes in river flow and establishment of non-indigenous species in
estuaries
The disruption of natural river flow regimes affects biological communities
along hundreds of kilometers across a spectrum of habitats, both aquatic
and terrestrial, and even including adjacent coastal areas. Dams, water
diversion, water extraction, and climate change are the factors most known
for altering natural river flow regimes. The impacts caused by these factors
on established ecological dynamics may create the opportunities for non-
indigenous species to establish or to become invasive (McAllister et al. 2001).
Indeed, the Guadiana estuary underwent profound changes in all aspects
of its geological, physical, chemical, and biological dynamics since the
completion of the Alqueva dam in 2002 (Morais 2007, 2008; Morais et al.
2009; Domingues et al. 2011, 2014; Garel and D’Alimonte 2017). For
example, the reduction of river flow increased the salinity along the estuary
and the number of marine species present. Previously, the middle estuary
was characterized by a reduced number of species mainly due to salinity
constraints owing to marked salinity variations along the year at the
estuarine turbidity maximum (Chícharo et al. 2001; Morais et al. 2009; Garel
and Ferreira 2011). Nowadays, the estuarine turbidity maximum shifted
more than 10 km upstream in comparison to pre-dam conditions and
salinity conditions became more stable throughout the year (Morais 2007;
Garel and D’Alimonte 2017). The new abiotic conditions resulted in empty
ecological niches which coincided with an increase in the number of non-
indigenous species identified over recent years in this part of the river: e.g.,
Cordylophora caspia (Pallas, 1771) (Cnidaria, Hydrozoa) (Seyer et al. 2017),
Synidotea laticauda (Crustacea, Isopoda) (Mellado-Díaz et al. 2018), oriental
shrimp Palaemon macrodactylus Rathbun, 1902 (Crustacea, Caridea)
(Chícharo et al. 2009), weakfish Cynoscion regalis (Bloch and Schneider,
1801) (Pisces, Sciaenidae) (Morais and Teodósio 2016), and now the
Atlantic blue crab (this study).
We hypothesize that the increased salinity observed in the middle and
the lower reaches of the upper Guadiana estuary made these areas available
for the colonization of native species, but it also presented an opportunity
for non-indigenous species to establish viable populations (Seyer et al.
2017). The most likely mechanisms associated with the introduction of the
Atlantic blue crab into the Guadiana estuary are probably due to the
reduced abiotic and/or biotic resistance in these newly available niches
(Procheş et al. 2008; Taylor and Duggan 2011; Papacostas et al. 2017), as
we hypothesize that propagule pressure is not the cause for the
introduction and putative establishment of the Atlantic blue crab in the
Guadiana estuary. A reversed scenario was observed for the invasive
porcelain crab Petrolisthes armatus (Gibbers, 1850) (Decapoda, Anomura)
New records of the Atlantic blue crab in the Iberian Peninsula
Morais et al. (2019), BioInvasions Records (in press)7
in Georgia (USA) where the propagule pressure overwhelmed the native
biotic resistance (Hollebone and Hay 2007).
Therefore, and as part of a future research framework, this hypothesis
must be tested and the case of the porcelain crab used as an example of the
opposite scenario.
Overlap with native Brachyura
The Ria Formosa lagoon is a mosaic of different benthic habitats, mainly of
muddy and sandy bottoms and of submerged aquatic vegetation patches.
Salinity changes across its extension are minimal, except during episodic
rain events. Here, the most abundant Brachyurans are the West African
fiddler crab Uca tangeri (Eydoux, 1835) (Wolfrath 1992), the marbled rock
crab Pachygrapsus marmoratus (Fabricius, 1787), and the European green
crab Carcinus maenas (Linnaeus, 1758) (Sprung 2001). Hypothetically, these
species could hinder the invasion of the Atlantic blue crab if their niches
overlap. However, the Atlantic blue crab has plenty of habitats available
along the Ria Formosa lagoon which increases their chances of establishment,
as it seems to be the case. Nonetheless, only a future sistematic assessment
across the entire lagoon can confirm or discredit this hypothesis.
In estuarine ecosystems like the Guadiana estuary, the diversity of
species tends to decrease upstream towards oligohaline areas, and then to
increase again towards freshwater areas – Remane diagram sensu Whitfield
et al. (2012). In this estuary, the Atlantic blue crab was collected mainly in
the middle estuary (between 12 and 20 km from the river mouth) and in
the lower section of the upper estuary (from 20 km upstream the river
mouth). At least other three Brachyura species are present in the Guadiana
estuary. The flying crab Liocarcinus holsatus (Fabricius, 1787) (Encarnação
et al. 2013) and marbled rock crab Pachygrapsus marmoratus (Fabricius,
1787) are present exclusively in the lower estuary (up to 12 km upstream
the river mouth), while the European green crab Carcinus maenas
(Linnaeus, 1758) is present both in the lower and middle estuary
(Encarnação et al. 2013). Occasionally, species of the genus Liocarcinus
might be present near the river mouth. Thus, the Atlantic blue crab has a
broader upstream distribution in this estuary than any other Brachyura.
However, most of Atlantic blue crab currently known distribution range
overlaps with the upper distribution range of the European green crab.
Therefore, competition and functional redundancy could be high between
the native European green crab and the Atlantic blue crab if this non-
indigenous species will ever reach an invasive status. Nonetheless, the
upper estuarine region is, without doubt, the area where the Atlantic blue
crab will face less competition with native Brachyurans.
The co-existence of the Atlantic blue crab and European green crab in
the Ria Formosa lagoon and in the Guadiana estuary, as well as in the
New records of the Atlantic blue crab in the Iberian Peninsula
Morais et al. (2019), BioInvasions Records (in press)8
northwestern Atlantic is an open avenue for experimental studies on
fundamental invasion ecology since both species are native and invasive in
opposite regions of the North Atlantic. It is worth mentioning that the
intraguild competition between native blue crab and non-indigenous green
crab is modulated by temperature-dependent interactions as observed in a
mesocosms experiment (Rogers et al. 2018). At low temperatures, green
crabs preyed upon blue crabs, while at higher temperatures similar size
blue and green crabs had similar competition capabilities but bigger blue
crabs preyed upon green crabs (Rogers et al. 2018). A field study in the
NW-Atlantic showed that the native blue crab controlled the green crab
invasion, since the abundance of green crabs was controlled by the
abundance of blue crabs (deRivera et al. 2005). Therefore, any extrapolations
from these observations to the Ria Formosa lagoon and the Guadiana
estuary—and to any other location where the Atlantic blue crab is non-
indigenous—is highly speculative at least for three main reasons: 1) each
site has its intrinsic abiotic and biotic specificities; 2) different lineages may
be involved in the invasion so the outcome of species interactions vary (see
Morais and Reichard (2018) for a review on cryptic invasions); 3) the time
elapsed since the introduction of the NIS influences the naivety of native
species towards the NIS behavior and therefore the outcomes of species
interaction (Reichard et al. 2015). Thus, research on the fundamental
invasion ecology of the Atlantic blue crab constitutes a third topic of our
proposed research framework.
The Atlantic blue crab as a fishing resource
The introduction of the Atlantic blue crab increases the number of edible
non-indigenous species present in the area, and particularly in the
Guadiana estuary. Probably, the most notorious edible non-indigenous
species present in this estuary is weakfish (Morais and Teodósio 2016;
Morais et al. 2017). The use of the Atlantic blue crab as a new fishing
resource in its non-indigenous range was already proposed and described
extensively (Mancinelli et al. 2017b), which might become a reality if the
species would ever reach an invasive status in the Ria Formosa lagoon or in
the Guadiana estuary. However, there are some caveats in using non-
indigenous species, and particularly invasive species, as a food resource,
and how this use may mitigate their putative negative effects upon
ecosystems (Nuñez et al. 2012). Thus, there are three main aspects to
consider, as already pointed out for weakfish (Morais et al. 2017). First,
fishing pressure must efficiently reduce the non-indigenous species
population size and growth without affecting other native species (Nuñez
et al. 2012). Second, the public must be made aware of the putative
negative impacts of non-indigenous species and that introductions into
non-invaded areas are not permitted (Nuñez et al. 2012). Third, the fishery
New records of the Atlantic blue crab in the Iberian Peninsula
Morais et al. (2019), BioInvasions Records (in press)9
of an invasive species can never be managed to make it sustainable (Nuñez
et al. 2012), which disables local communities from obtaining a long-term
financial revenue. However, we advocate that the Atlantic blue crab fishery
must be regulated in a near future if there is an opportunity to become
sustainable, but only if it does not jeopardize existing fisheries and the
ecosystem. Local communities should be the sole beneficiaries of this
complementary revenue, which would avoid increased fishing pressure and
other impacts induced by fishers coming from other regions. Any legal
aspects regarding the use of non-indigenous species, and of invasive
species in particular, should deserve an objective but thorough case-by-
case assessment.
Acknowledgements
PM has a scholarship funded by the Delta Stewardship Council and Delta Science Program
under Grant No. (1167). The contents of this material do not necessarily reflect the views and
policies of the Delta Stewardship Council, nor does mention of trade names or commercial
products constitute endorsement or recommendation for use. MAT was funded by Foundation
for Science and Technology (FCT, Portugal) through the project UID/Multi/04326/2013, and by
the European Regional Development Fund (COMPETE program- Operational Competitiveness
Programme). The work of EG was supported by FCT research contract IF/00661/2014/CP1234,
VB (SFRH/BD/104209/2014), and FL (SFRH/BPD/108949/2015) hold scholarships funded by
FCT. Data Collection was partially supported by the Project No. 16-01-04-FMP-0005:
CRUSTAPANHA - Contribution to the sustainable management of small-scale fisheries of
crustaceans: Study of ecology, biology and population dynamics of small crabs with interest
commercial development along the Portuguese coast (Operational Program MAR2020). The
authors also acknowledge the contributions of two anonymous reviewers which helped
improved an initial version of this paper. Publication made possible in part by support from the
Berkeley Research Impact Initiative (BRII) sponsored by the UC Berkeley Library.
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Supplementary material
The following supplementary material is available for this article:
Table S1. Records of Atlantic blue crab Callinectes sapidus Rathbun, 1896 collected in the Ria Formosa lagoon and Guadiana estuary
(SW Iberian Peninsula) by local fishermen in 2017 and up to June 2018. The number of specimens collected (N), carapace width (cm),
total fresh weight (g), and sex (M – male, F – female, or undetermined) are described.
Table S2. Temperature and salinity measured in the Guadiana estuary at four sampling stations and three different depths during neap
(August 31, 2017) and spring tides (September 8, 2017).
