The first invasive bivalve in African fresh waters: invasion portrait
and management options
MIGUEL CLAVEROa,*, RAFAEL ARAUJOb, JAVIER CALZADAc, MIGUEL DELIBESa, NÉSTOR FERNÁNDEZa,
CARLOS GUTIÉRREZ-EXPÓSITOa,d, ELOY REVILLAa and JACINTO ROMÁNa
a
Estación Biológica de Doñana, CSIC, Américo Vespucio s/n, 41092 Sevilla, Spain bMuseo Nacional
de Ciencias Naturales, CSIC, José Gutiérrez Abascal 2, 28006 Madrid, Spain cDepartamento de
Biología Ambiental y Salud Pública, Universidad de Huelva, 21071 Huelva, Spain
d
Área de Conservación, Espacio Natural Doñana, Centro Administrativo El Acebuche, 21760 Matalascañas, Spain
ABSTRACT
1. The first clear evidence of the establishment of an invasive freshwater bivalve in Africa is provided, through
the description of the distribution of Corbicula fluminea in Morocco.
2. C. fluminea was detected in 2008 and 2011 in two independent river basins, although still absent in other river
systems throughout the country.
3. This information is used to propose management actions, which should be focused on avoiding interbasin
expansion as well as new introduction events from European fresh waters.
KEY WORDS:
river; reservoir; introduction; distribution; invertebrates; alien species
Bivalves, together with fish and crayfish, are one of
the main groups of freshwater invaders. Invasive
bivalves have been shown to threaten native species
(Ricciardi et al., 1996) and may have large impacts
on the biodiversity and functioning of aquatic
systems (Sousa et al., 2008, 2009). These impacts
have been widely reported from several places
around the world, but not yet in Africa. Recent
assessments of the status of freshwater biodiversity in
Africa considered freshwater bivalve invasion to be a
non-existent problem in the continent (Van Damme
et al., 2010; Seddon et al., 2011).
The genus Corbicula has a wide distribution,
enclosing tropical and subtropical areas in Africa,
Asia, the Malay Archipelago, the Philippines
and Eastern Australia (Glaubrecht et al., 2007;
Figure 1(A)). In Africa, it occurs from Egypt
and Ethiopia to Senegal and southwards to
South Africa, but is naturally absent from large
areas of the north-west part of the continent
(Mandahl-Barth, 1988). The genus seems to be a
latecomer in Africa, recorded in the fossil record
from the Lower or Mid Pliocene, but has become a
dominant bivalve genus in fresh waters across
Sudanian Africa (Van Damme, 1984). In the early
20th century Corbicula clams were introduced to
North America, arriving in South America and
Europe during the second half of the century
(Karatayev et al., 2007). Corbicula species behave
as invaders in their non-native range, rapidly
*Correspondence to: M. Clavero, Estación Biológica de Doñana, CSIC. Américo Vespucio s/n, 41092 Sevilla, Spain. E-mail: miguelclavero@ebd.csic.es
Figure 1. (A) Native (light grey) and introduced (dark grey) ranges of the genus Corbicula, adapted with updates from Glaubrecht et al. (2007). The
arrow marks the approximate location of the new records of C. fluminea in northern Africa. (B) Current known range of C. fluminea in Morocco,
resulting from 124 surveys performed between 2008 and 2011. Filled dots denote localities with presence of the species, while empty dots denote places
in which it was not detected.
expanding their distribution and often attaining
large population densities (Araujo et al., 1993;
Karatayev et al., 2003; Sousa et al., 2008).
This note reports the first evidence of a
freshwater bivalve invasion in Africa, through the
description of the current distribution of Corbicula
fluminea in Morocco. Field data were obtained
through freshwater mussel surveys developed in
2008 and 2009 in 23 river stretches, and in an otter
(Lutra lutra) survey undertaken in 2011 during
which 101 river stretches were visited. Only
presence–absence data are presented, since no
quantitative assessment of C. fluminea populations
was made. Mussel surveys involved intensive
searches for freshwater bivalves, which were
collected by a team of four people by wading and
occasionally using a water-scoop or snorkelling.
Otter surveys focused on the search for otter signs
(scats or footprints), undertaken by three or four
persons along 600 m of river shore (Delibes et al.,
in press). During these surveys samples of bivalve
specimens (fresh parts and shells) of the different
species detected, including those of C. fluminea,
were also collected. Although molecular analyses
for species identification have not yet been carried
out, shell morphological features strongly match
those of the common Asian clam C. fluminea.
Current known distribution of C. fluminea in
Morocco is restricted to the northwest of the
country, expanding throughout the Sebou River
basin, including the Sebou itself and its tributaries
Beth and Inaouen, and through the Oum Er-Rbia
River (Figure 1(B)). The species was detected in
the two basins through the surveys of mussels and
otters, supporting the accuracy of the description
of current range. River stretches occupied by
C. fluminea tend to be wide watercourses placed at
low altitudes (below 200 masl). The occurrence
of the species seems to be related to the presence
of reservoirs, whether upstream or downstream.
C. fluminea is apparently absent from Mediterranean
Moroccan rivers, since no specimens were found
during specific bivalve surveys in 2009 or during an
otter survey carried out in 2011. Although we do
not have information about Algerian rivers, the
species has not yet been recorded in Tunisian ones
(N. Khalloufi pers. com.).
The introduction of C. fluminea into Morocco
is probably related to fish stocking, whether
for aquaculture or sport fishing purposes. The
relationships in the development of aquaculture
between Morocco and Spain could have favoured
the introduction of C. fluminea, since the species is
present now in many Iberian basins (Pérez-Quintero,
2008), some of which hold important aquaculture
centres. Many aquaculture resources in Morocco,
including juveniles of several farmed fish species,
are imported from Spain (FAO, 2008–2011).
Furthermore, the Moroccan administration also
performs fish stocking, involving mostly non-native
species, to promote sport fishing. Specifically, several
non-native fish species have been stocked in different
areas of the Sebou Basin (El Madani and
Strosser, 2008). These fish stockings could be
related to the introduction and subsequent spread
of C. fluminea. Movement of machinery between
Europe and Morocco related to dam construction,
channelization or other human interventions on
rivers may also have been involved in the arrival
of C. fluminea in Africa.
The ecological and economic impacts of
C. fluminea in invaded freshwater systems,
applicable also to Moroccan ones, have recently
been reviewed by Karatayev et al. (2007) and Sousa
et al. (2008). C. fluminea could become a new threat
for native Northern African unionids, some of
which are already globally threatened (e.g. the
critically endangered Margaritifera marocana or the
endangered Potomida littoralis). C. fluminea has
been shown to have negative effects on the growth
and survival of juvenile unionids (Vaughn
and Spooner, 2006). Moreover, when attaining
high densities C. fluminea can suffer massive
mortality episodes (Ilarri et al., 2011), during which
a large amount of ammonia is released, often
surpassing acute tolerance levels for unionids
(Cherry et al., 2005). The spread of C. fluminea
within Africa could also put in contact invasive
and native Corbicula populations, the nearest of
the latter being found in Senegal (Sarr et al.,
2011; Figure 1).
C. fluminea seems well established in the Sebou and
Oum Er-Rbia basins, where eradication or control
actions may not be feasible. In these basins, species
distribution should be monitored, in order to allow
the early detection of new populations. Authorities
should take measures to avoid the human-mediated
colonization of non-occupied sectors of the basins,
especially focusing on upstream movements and
naturally inaccessible systems such as upstream
reservoirs. This could be achieved by avoiding
water movements from colonized areas, especially
through irrigation, boats, machinery and fish tanks
(Durán et al., 2010).
From a wider perspective, the invasion of
C. fluminea in Northern Africa is still in its
initial stages. Taking advantage of the relatively
localized current distribution range of C. fluminea,
Moroccan
environmental
authorities
should
implement measures to avoid further spread to
other basins. This should be a priority given the
probable ecological and economic impacts of the
species. Movements of water and sediments in any
form from the Sebou and Oum Er-Rbia basins to
other areas should be avoided whenever possible,
and subjected to strict controls when unavoidable.
This includes boats and outboard motors, fish
movements, civil works or water diversions, among
others. The species has the potential to spread
throughout other African freshwater systems in
future as has occurred in other areas colonized
(Den Hartog et al., 1992).
Finally, the arrival of C. fluminea to African
fresh waters is a clear wake-up call for the
possibility of new introductions. Other highly
invasive bivalve species, such as the zebra
mussel (Dreissena polymorpha) and the Chinese
pond mussel (Anodonta woodiana) are currently
present and expanding their ranges in the Iberian
Peninsula. The case of the zebra mussel is especially
worrying, since the species is already present in
south Iberian river basins (Guadalquivir River), it
has a large expansion potential and it produces
huge ecosystem-level and economic impacts
(Strayer, 2009). The Strait of Gibraltar has proved
not to be an effective barrier for freshwater bivalve
dispersal, and thus the Iberian–Morocco connection
could become an invasion route for freshwater
bivalves into Africa. We hope that the finding of
C. fluminea in Morocco will serve at least to initiate
measures to prevent the arrival of the zebra mussel
in Africa.
ACKNOWLEDGEMENTS
We are grateful to Dr Abdeljebbar Qninba for
facilitating our field work in Morocco. Permission
for sampling was obtained from the Haut
Commissariat aux Eaux et Forêts et a la Lutte
contre la Désertification du Royaume du Maroc.
S. Alvaré, A. Machordom, J. Reis, J.M. Barea,
280
M. CLAVERO ET AL.
M. Ghamizi and M. J. Madeira helped us with the
field work and Sofía Conradi collaborated in
many ways. Comments made by R. Sousa and an
anonymous referee helped to improve the manuscript.
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