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Ouémé River Basin, Benin) and Comparison Within S diversity Article Molecular Identification of an Invasive Sarotherodon Species from the Atchakpa Freshwater Reservoir (Ouémé River Basin, Benin) and Comparison within S. melanotheron Using COI Markers Rodrigue Orobiyi Edéya Pèlèbè 1,2,* , Ibrahim Imorou Toko 1 , Erik Verheyen 3,4 and Maarten Van Steenberge 3 1 Research Laboratory in Aquaculture and Aquatic Ecotoxicology (LaRAEAq), Faculty of Agronomy (FA), University of Parakou (UP), P.O. Box 61 Parakou-University, Parakou, Benin; [email protected] 2 World Bank Africa Centre of Excellence in Coastal Resilience (ACECoR), University of Cape Coast (UCC), Ground Floor C. A. Ackah Lecture Theatre Complex, Cape Coast, Ghana 3 Operational Directorate (OD) Taxonomy and Phylogeny, Royal Belgian Institute for Natural Sciences (RBINS), Vautierstraat 29, 1000 Brussels, Belgium; [email protected] (E.V.); [email protected] (M.V.S.) 4 Department Biology, Evolutionary Ecology, University of Antwerp, Universiteitsplein 1, 2610 Antwerpen, Belgium * Correspondence: [email protected] or [email protected]; Tel.: +229-96-97-57-62 or +233-(0)-055-242-8692 Abstract: The Atchakpa freshwater reservoir (Ouémé Basin, Benin) was found to harbour an unex- Citation: Pèlèbè, R.O.E.; Imorou pected population of a cichlid species that was presumed to be Sarotherodon melanotheron. This species Toko, I.; Verheyen, E.; Van Steenberge, became dominant in the reservoir and became the main fisheries target species. We applied DNA M. Molecular Identification of an barcoding to identify this population. Besides specimens from the reservoir, we also sequenced S. Invasive Sarotherodon Species from melanotheron from its native range in Benin at the lower Ouémé and Sô Rivers, and from Lake Nokoué, the Atchakpa Freshwater Reservoir and Porto-Novo Lagoon. High sequence similarity indicated that all specimens were conspecific. (Ouémé River Basin, Benin) and Hence, we cannot exclude that a natural range extension led to the presence of the species in the Comparison within S. melanotheron reservoir. A comparison with sequences from NCBI GenBank confirmed that all samples belonged to Using COI Markers. Diversity 2021, S. m. melanotheron 13, 297. https://doi.org/10.3390/ the subspecies , which is native to Benin. This comparison also showed that this d13070297 subspecies was previously introduced in the Philippines. We call for further studies to investigate the socioeconomic, ecological and environmental impacts of the species in the Atchakpa reservoir. Academic Editors: Stephan Koblmüller and Michael Wink Keywords: cytochrome c oxidase subunit I; black-chin tilapia; DNA barcoding; Savè; species introductions Received: 14 May 2021 Accepted: 29 June 2021 Published: 30 June 2021 1. Introduction Publisher’s Note: MDPI stays neutral The black-chin tilapia, Sarotherodon melanotheron (Rüppell, 1852), is an estuarine species with regard to jurisdictional claims in endemic to West and Central Africa [1–3] that is well known from the brackish waters of published maps and institutional affil- southern Benin. In the Ouémé River basin, its limit of frequent occurrence is the village iations. of Agonlin-Lowé (Commune of Adjohoun, department of Ouémé)[4]. This locality is considered the boundary between the continental and the coastal domains in Benin [4] (Figure1). However, rare specimens of S. melanotheron have been found upstream of Agonlin-Lowé in southern Benin (rare occurrences at the Ouémé River at Toué, Commune Copyright: © 2021 by the authors. of Covè, department of Zou [4], at the Hlan River at Lokoli, Commune of Zogbodomey, Licensee MDPI, Basel, Switzerland. department of Zou [5] and in the Lake Hlan at Kpomè, Commune of Toffo, department of This article is an open access article Atlantic [6]) (Figure1). distributed under the terms and A large population of presumed S. melanotheron was discovered prior to 2001 in the conditions of the Creative Commons Atchakpa freshwater reservoir (SUCOBE dam built in 1982), which is located in central Attribution (CC BY) license (https:// Benin, about 230 km north of Agonlin-Lowé [4,7]. This population, which was only creativecommons.org/licenses/by/ morphologically identified, thrived in the landlocked reservoir. Despite its proximity to 4.0/). Diversity 2021, 13, 297. https://doi.org/10.3390/d13070297 https://www.mdpi.com/journal/diversity Diversity 2021, 13, x FOR PEER REVIEW 2 of 10 Diversity 2021, 13, 297 2 of 10 morphologically identified, thrived in the landlocked reservoir. Despite its proximity to thethe mainmain coursecourse ofof thethe OuOuéméémé River,River, thethe reservoirreservoir hashas nono directdirect connectionconnection withwith thethe riverriver (Figure(Figure2 )2) although, although, during during severe severe dry dry seasons, season seasonals, seasonal contact contact with with river river water water can can occur oc- throughcur through pumping. pumping.S. melanotheron S. melanotheronis quasi-inexistent is quasi-inexistent at the at Ou theém Ouéméé River River nearthe near reservoir the res- aservoir only as one only individual one individual was captured was captured during threeduring years three of years intensive of intensive sampling sampling from 1998 from to 20011998 [to4]. 2001 Moreover, [4]. Moreover, the Atchakpa the Atchakpa fisheries fi managementsheries management committee committee has, in has, recent in years,recent notyears, reported not reported any catches any catches of this of species this specie in thes in Ou theém Ouéméé River River near thenear reservoir. the reservoir. If the If morphologicalthe morphological identifications identifications of [4, 7of] are[4,7] correct, are correct, this population this population is isolated is isolated from the from rest the of itsrest natural of its natural geographic geographic distribution distribution in Benin. in Benin. FigureFigure 1.1. Hydrographic map map of of Benin Benin showing showing the the Ouém Ouémé Riveré River basin, basin, with with the the location location of the of the Atchakpa reservoir, the sampling stations, the limit of frequent occurrence and the localities of Atchakpa reservoir, the sampling stations, the limit of frequent occurrence and the localities of rare rare occurrences of S. melanotheron. occurrences of S. melanotheron. Diversity 2021, 13, x FOR PEER REVIEW 3 of 10 The fisheries in the Atchakpa reservoir ensure the supply of fish for the city of Savè. Currently, the population morphologically identified as S. melanotheron dominates the catches of local fishermen in terms of abundance. According to [8], S. melanotheron repre- sents 72% (numerical abundance) of the fish caught at the Atchakpa reservoir and sold at the fish market in Savè. It thus surpasses the Nile tilapia Oreochromis niloticus (Linnaeus, Diversity 2021, 13, 297 1758), which was introduced into the reservoir through aquaculture (direct restocking3 of in 10 1985 and cage culture in 2014). Nile tilapia is currently rare whereas it was very common in the 1990s. Atchakpa Ouémé water River reservoir Figure 2. Satellite image highlighting the absence of direct communication between the main course of the Ouémé River Figure 2. Satellite image highlighting the absence of direct communication between the main course of the Ouémé River and the Atchakpa freshwater reservoir (source: Google maps). and the Atchakpa freshwater reservoir (source: Google maps). Sarotherodon melanotheron is known to be invasive, i.e., it has the potential to spread The fisheries in the Atchakpa reservoir ensure the supply of fish for the city of Savè. widely, reproduce rapidly and persist in a new environment with a large range of impacts Currently, the population morphologically identified as S. melanotheron dominates the [9,10]. Knowing the correct identity of an invasive species is an important prerequisite for catches of local fishermen in terms of abundance. According to [8], S. melanotheron repre- itssents efficient 72% (numericalmanagement. abundance) The identification of the fish of caught invasive at thecichlids Atchakpa using reservoironly metric and and sold me- at risticthe fish parameters market in requires Savè. It caution thus surpasses due to th theeir Nile mega-diversity tilapia Oreochromis and the niloticuswidespread(Linnaeus, intro- duction1758), which of alien was species introduced [11,12]. into Therefore, the reservoir molecular through evidence aquaculture is often (directrequired restocking to provide in additional1985 and cage verification. culture in Hence, 2014). we Nile chose tilapia to, isfor currently the first time rare whereasin Beninese it was fisheries, very common apply a DNAin the barcoding 1990s. approach. DNA barcoding is a molecular technique for fast and accurate determinationSarotherodon of species melanotheron identityis known[13]. In toanimals, be invasive, DNA i.e.,barcoding it has the is potentialusually performed to spread bywidely, sequencing reproduce a fragment rapidly of andthe mitochondr persist inial a newcytochrome environment c oxidase with subunit a large I gene, range COI of (barcode),impacts [9 of,10 the]. Knowing specimen the under correct investigatio identity ofn and an invasiveits comparison species with is an a important reference library prereq- ofuisite barcode for its sequences efficient management. [14,15]. The identification of invasive cichlids using only metric andSarotherodon meristic parameters melanotheron requires contains caution substantial due to their intra-specific mega-diversity geographic and the widespread structure, withintroduction
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