SHORT COMMUNICATION

The first invasive bivalve in African fresh waters: invasion portraitand management options

MIGUEL CLAVEROa,*, RAFAEL ARAUJOb, JAVIER CALZADAc, MIGUEL DELIBESa, NÉSTOR FERNÁNDEZa,CARLOS GUTIÉRREZ-EXPÓSITOa,d, ELOY REVILLAa and JACINTO ROMÁNa

aEstación Biológica de Doñana, CSIC, Américo Vespucio s/n, 41092 Sevilla, SpainbMuseo Nacional de Ciencias Naturales, CSIC, José Gutiérrez Abascal 2, 28006 Madrid, Spain

cDepartamento de Biología Ambiental y Salud Pública, Universidad de Huelva, 21071 Huelva, SpaindÁrea 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, throughthe 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 riversystems throughout the country.

3. This information is used to propose management actions, which should be focused on avoiding interbasinexpansion as well as new introduction events from European fresh waters.Copyright # 2012 John Wiley & Sons, Ltd.

Received 24 November 2011; Revised 12 January 2012; Accepted 22 January 2012

KEY WORDS: river; reservoir; introduction; distribution; invertebrates; alien species

Bivalves, together with fish and crayfish, are one ofthe main groups of freshwater invaders. Invasivebivalves have been shown to threaten native species(Ricciardi et al., 1996) and may have large impactson the biodiversity and functioning of aquaticsystems (Sousa et al., 2008, 2009). These impactshave been widely reported from several placesaround the world, but not yet in Africa. Recentassessments of the status of freshwater biodiversity inAfrica considered freshwater bivalve invasion to be anon-existent problem in the continent (Van Dammeet 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 Egyptand Ethiopia to Senegal and southwards toSouth Africa, but is naturally absent from largeareas of the north-west part of the continent(Mandahl-Barth, 1988). The genus seems to be alatecomer in Africa, recorded in the fossil recordfrom the Lower or Mid Pliocene, but has become adominant bivalve genus in fresh waters acrossSudanian Africa (Van Damme, 1984). In the early20th century Corbicula clams were introduced toNorth America, arriving in South America andEurope during the second half of the century(Karatayev et al., 2007). Corbicula species behaveas invaders in their non-native range, rapidly

*Correspondence to: M. Clavero, Estación Biológica de Doñana, CSIC. Américo Vespucio s/n, 41092 Sevilla, Spain. Email: miguelclavero@ebd.csic.es

Copyright # 2012 John Wiley & Sons, Ltd.

AQUATIC CONSERVATION: MARINE AND FRESHWATER ECOSYSTEMS

Aquatic Conserv: Mar. Freshw. Ecosyst. (2012)

Published online in Wiley Online Library(wileyonlinelibrary.com). DOI: 10.1002/aqc.2231

expanding their distribution and often attaininglarge population densities (Araujo et al., 1993;Karatayev et al., 2003; Sousa et al., 2008).

This note reports the first evidence of afreshwater bivalve invasion in Africa, through thedescription of the current distribution of Corbiculafluminea in Morocco. Field data were obtainedthrough freshwater mussel surveys developed in2008 and 2009 in 23 river stretches, and in an otter(Lutra lutra) survey undertaken in 2011 duringwhich 101 river stretches were visited. Onlypresence–absence data are presented, since noquantitative assessment of C. fluminea populationswas made. Mussel surveys involved intensivesearches for freshwater bivalves, which werecollected by a team of four people by wading andoccasionally using a water-scoop or snorkelling.Otter surveys focused on the search for otter signs(scats or footprints), undertaken by three or fourpersons along 600m of river shore (Delibes et al.,in press). During these surveys samples of bivalvespecimens (fresh parts and shells) of the different

species detected, including those of C. fluminea,were also collected. Although molecular analysesfor species identification have not yet been carriedout, shell morphological features strongly matchthose of the common Asian clam C. fluminea.

Current known distribution of C. fluminea inMorocco is restricted to the northwest of thecountry, expanding throughout the Sebou Riverbasin, including the Sebou itself and its tributariesBeth and Inaouen, and through the Oum Er-RbiaRiver (Figure 1(B)). The species was detected inthe two basins through the surveys of mussels andotters, supporting the accuracy of the descriptionof current range. River stretches occupied byC. fluminea tend to be wide watercourses placed atlow altitudes (below 200 masl). The occurrenceof the species seems to be related to the presenceof reservoirs, whether upstream or downstream.C. fluminea is apparently absent from MediterraneanMoroccan rivers, since no specimens were foundduring specific bivalve surveys in 2009 or during anotter survey carried out in 2011. Although we do

Figure 1. (A) Native (light grey) and introduced (dark grey) ranges of the genus Corbicula, adapted with updates from Glaubrecht et al. (2007). Thearrow 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.

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Copyright # 2012 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. (2012)

not have information about Algerian rivers, thespecies has not yet been recorded in Tunisian ones(N. Khalloufi pers. com.).

The introduction of C. fluminea into Moroccois probably related to fish stocking, whetherfor aquaculture or sport fishing purposes. Therelationships in the development of aquaculturebetween Morocco and Spain could have favouredthe introduction of C. fluminea, since the species ispresent now in many Iberian basins (Pérez-Quintero,2008), some of which hold important aquaculturecentres. Many aquaculture resources in Morocco,including juveniles of several farmed fish species,are imported from Spain (FAO, 2008–2011).Furthermore, the Moroccan administration alsoperforms fish stocking, involving mostly non-nativespecies, to promote sport fishing. Specifically, severalnon-native fish species have been stocked in differentareas of the Sebou Basin (El Madani andStrosser, 2008). These fish stockings could berelated to the introduction and subsequent spreadof C. fluminea. Movement of machinery betweenEurope and Morocco related to dam construction,channelization or other human interventions onrivers may also have been involved in the arrivalof C. fluminea in Africa.

The ecological and economic impacts ofC. fluminea in invaded freshwater systems,applicable also to Moroccan ones, have recentlybeen reviewed by Karatayev et al. (2007) and Sousaet al. (2008). C. fluminea could become a new threatfor native Northern African unionids, some ofwhich are already globally threatened (e.g. thecritically endangered Margaritifera marocana or theendangered Potomida littoralis). C. fluminea hasbeen shown to have negative effects on the growthand survival of juvenile unionids (Vaughnand Spooner, 2006). Moreover, when attaininghigh densities C. fluminea can suffer massivemortality episodes (Ilarri et al., 2011), during whicha large amount of ammonia is released, oftensurpassing acute tolerance levels for unionids(Cherry et al., 2005). The spread of C. flumineawithin Africa could also put in contact invasiveand native Corbicula populations, the nearest ofthe latter being found in Senegal (Sarr et al.,2011; Figure 1).

C. fluminea seems well established in the Sebou andOum Er-Rbia basins, where eradication or controlactions may not be feasible. In these basins, speciesdistribution should be monitored, in order to allowthe early detection of new populations. Authoritiesshould take measures to avoid the human-mediatedcolonization of non-occupied sectors of the basins,

especially focusing on upstream movements andnaturally inaccessible systems such as upstreamreservoirs. This could be achieved by avoidingwater movements from colonized areas, especiallythrough irrigation, boats, machinery and fish tanks(Durán et al., 2010).

From a wider perspective, the invasion ofC. fluminea in Northern Africa is still in itsinitial stages. Taking advantage of the relativelylocalized current distribution range of C. fluminea,Moroccan environmental authorities shouldimplement measures to avoid further spread toother basins. This should be a priority given theprobable ecological and economic impacts of thespecies. Movements of water and sediments in anyform from the Sebou and Oum Er-Rbia basins toother areas should be avoided whenever possible,and subjected to strict controls when unavoidable.This includes boats and outboard motors, fishmovements, civil works or water diversions, amongothers. The species has the potential to spreadthroughout other African freshwater systems infuture as has occurred in other areas colonized(Den Hartog et al., 1992).

Finally, the arrival of C. fluminea to Africanfresh waters is a clear wake-up call for thepossibility of new introductions. Other highlyinvasive bivalve species, such as the zebramussel (Dreissena polymorpha) and the Chinesepond mussel (Anodonta woodiana) are currentlypresent and expanding their ranges in the IberianPeninsula. The case of the zebra mussel is especiallyworrying, since the species is already present insouth Iberian river basins (Guadalquivir River), ithas a large expansion potential and it produceshuge ecosystem-level and economic impacts(Strayer, 2009). The Strait of Gibraltar has provednot to be an effective barrier for freshwater bivalvedispersal, and thus the Iberian–Morocco connectioncould become an invasion route for freshwaterbivalves into Africa. We hope that the finding ofC. fluminea in Morocco will serve at least to initiatemeasures to prevent the arrival of the zebra musselin Africa.

ACKNOWLEDGEMENTS

We are grateful to Dr Abdeljebbar Qninba forfacilitating our field work in Morocco. Permissionfor sampling was obtained from the HautCommissariat aux Eaux et Forêts et a la Luttecontre la Désertification du Royaume du Maroc.S. Alvaré, A. Machordom, J. Reis, J.M. Barea,

INVASIVE CORBICULA IN AFRICA

Copyright # 2012 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. (2012)

M. Ghamizi and M. J. Madeira helped us with thefield work and Sofía Conradi collaborated inmany ways. Comments made by R. Sousa and ananonymous referee helped to improve the manuscript.

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