Arxius de Miscel·lània Zoològica. Volumen 23 (2025) Páginas: 33-43
The Asian clam Corbicula fluminea in Ecuador: dispersion and diversity of occupied environments
Lodeiros, C., Gutiérrez Gregoric, D. E., González-Henríquez, N., Hernández-Reyes, D., Rey-Méndez, M., Panta-Vélez, R. P., Bernal-Zambrano, J. J., Darrigran, G.
DOI: https://doi.org/10.32800/amz.2025.23.0033Descargar
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Lodeiros, C., Gutiérrez Gregoric, D. E., González-Henríquez, N., Hernández-Reyes, D., Rey-Méndez, M., Panta-Vélez, R. P., Bernal-Zambrano, J. J., Darrigran, G., 2025. The Asian clam Corbicula fluminea in Ecuador: dispersion and diversity of occupied environments. Arxius de Miscel·lània Zoològica, 23: 33-43, DOI: https://doi.org/10.32800/amz.2025.23.0033-
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Abstract
The Asian clam Corbicula fluminea in Ecuador: dispersion and diversity of occupied environments
Populations of invasive species can have a negative impact on the natural environment and socioeconomic effects of artificial systems. The relationship of Corbicula fluminea with humans, together with the its great adaptive-reproductive capacity, make it one of the most expansive species of invasive bivalves worldwide. Here we report on the dispersion of C. fluminea, and based on genetic analysis we describe the presence and potentially negative effect of this species for the first time in an anthropic environment, an aquaculture facility in Ecuador.
Key words: Bivalve, Invasion, Effects, Impacts, Global distribution, Freshwater
Resumen
La almeja asiática Corbicula fluminea en Ecuador: dispersión y diversidad de ambientes ocupados
Las poblaciones de especies invasoras ocasionan impactos sobre el medio natural y efectos socioeconómicos sobre los sistemas artificiales. La relación que tiene la especie Corbicula fluminea con el ser humano, sumada a su gran capacidad adaptativa-reproductiva, la convierte en una de las más expansivas entre los bivalvos invasores del planeta. El presente estudio señala no solo la dispersión de C. fluminea sino también, a través del análisis genético, la presencia de esta especie por primera vez en un ambiente antrópico en Ecuador, una instalación de acuicultura, y el potencial efecto negativo sobre la misma.
Palabras claves: bivalvos, invasión, efectos, impactos, distribución global, agua dulce
Resum
La cloïssa asiàtica Corbicula fluminea a l’Equador: dispersió i diversitat d'ambients ocupats
Les poblacions d’espècies invasores generen impactes en el medi natural i efectes socioeconòmics en els sistemes artificials. La relació que estableix l’espècie Corbicula lumina amb l’ésser humà, a més de la gran capacitat adaptativa-reproductiva que té, la converteix en una de les més expansives entre els bivalves invasors del planeta. Aquest estudi no tan sols assenyala la dispersió de C. fluminea sinó també, mitjançant l’anàlisi genètica, la presència d’aquesta espècie per primera vegada en un ambient antròpic a l’Equador, una instal·lació d’aqüicultura, i el potencial efecte negatiu en aquesta.
Paraules clau: bivalves, invasió, efectes, impactes, distribució global, aigua dolça
Introduction
A species is considered invasive when it is detected outside its natural geographic area of dispersal, when it is capable of maintaining a self-sustaining population in that new ecosystem, and when it disperses extensively, causing not only an environmental impact but also having a socioeconomic effect (Diagne et al 2022).
Humans have historically transported species from one place to another, leading to two major increases in the exchange and transportation of non-native species, the first at the end of the Middle Ages and the second with the Industrial Revolution (Collado et al 2020). This trend has increased considerably in recent decades and is currently ongoing at a great magnitude and with great diversity from one point to another on the planet. Two factors favor this third increase in the transportation of non-native species. The first of these is globalization, with worldwide trade causing the 'sending' and 'receiving' of 'non-native species' to other regions of the world. (Hulme et al 2008, Hulme 2009). The second main factor is climate change, which impacts and favors the settlement of non-native species in receiving areas. These two factors act synergistically to increase the potential establishment of non-native species (Hess et al 2024). This phenomenon can have great environmental impact and cause significant economic effects. In aquatic ecosystems, the number of invasive species has increased significantly in in recent decades due to the close relationship of non-native species and human activities (Clusa et al 2017).
The Asian freshwater clam, Corbicula fluminea (Müller 1774), is one of the most expansive species of invasive bivalves because its high adaptive-reproductive capacity (Darrigran 2002, Vidinova et al 2021) has allowed it to invade all continents (table 1) except Antarctica (Gama et al 2016), dominating, both lentic and lotic environments worldwide (Darrigran 1992, Lucy et al 2012, Vidinova et al 2021). Given its invasiveness, in South America, its association with human activities (Sousa et al 2008) such as aquaculture, recreational activities such as bait for sports fishing, and transportation for human food, and through various transport vectors (table 2), C. fluminea has become the most invasive freshwater bivalve species in the continent (Darrigran et al 2020), causing significant adverse environmental impact. For example, several species of the genus Corbicula can impact hydrology, biogeochemical cycling and biotic interactions through wide-ranging mechanisms in individuals and ecosystems (Bespalaya et al 2021), and it may have economic effects such as macrofouling in industrial cooling systems (Darrigran 2002).
Table 1. Examples of global distribution of the mollusk Corbicula fluminea, one of the most invasive bivalve species of the 20th century.
Tabla 1. Ejemplos de distribución global del molusco Corbicula fluminea, una de las especies de bivalvos más invasoras del siglo XX.
Table 2. Potential vectors capable of dispersing Corbicula fluminea in South America.
Tabla 2. Vectores potenciales capaces de dispersar la especie Corbicula fluminea en América del Sur.
The origin of the invasive populations of C. fluminea poses a significant challenge due to the low genetic variability of its populations (Gomes et al 2016). In South America, two main invasion lineages have been detected (Gomes et al 2016, Ludwig et al 2024), with the invasive lineage (haplotype) FW5 (morphotype form A/R) showing the greatest distribution in Europe and America. The latter is followed by FW17 (morphotype form C/S), with an intermediate lineage in three sites in Brazil and a population with individuals that presented a new COI haplotype in Brazil (FWBra). Form A has a more trigonal shell, a higher and inflated umbos, thicker and more widely spaced external marginal ribs than form B (present in North America), and a lighter-colored inner shell surface. The form C morphotype has the finest external surface sculpture and the thinnest and least inflated shell of all three New World morphotypes. It is further distinguished from the co-occurring form A morphotype by the latter’s prominent umbo, posterior rostrum, and lighter coloration (Ituarte 1994, Lee et al 2005). The FWBra haplotype has shells with flatter umbos than the other morphotypes (Ludwig et al 2024).
In the present study, genetic analysis certified the presence of C. fluminea for the first time in an anthropic environment in Ecuador. Here we review the presence and dispersion of the species in South America.
Material and methods
The samples of C. fluminea were collected in November 2019 in the province of Manabí, Ecuador, in an aquaculture facility dedicated to the cultivation of the white shrimp Penaeus vannamei Boone, 1931 along with the Pacific fat sleeper fish, Dormitator latifrons (Richardson, 1844), located at the site La Isla, Pechichal commune, San Isidro parish, Sucre municipality (fig. 1; 0° 18' 05.6" S - 80° 11' 34.9" W). The shrimp produce is sent to packing facilities that export to various places worldwide, while the Pacific fat sleeper is exported to Asia or meets local demands.
Fig. 1. Extraction site of the invasive species Corbicula fluminea. Aquaculture system dedicated to the cultivation of white shrimp Penaeus vannamei and Pacific fat sleeper fish Dormitator latifrons, in La Isla, Pechichal commune, San Isidro parish, Sucre municipality, Manabí province, Ecuador.
Fig. 1. Lugar de extracción de la especie invasora Corbicula fluminea. Sistema acuícola dedicado al cultivo del camarón patiblanco Penaeus vannamei, y del chalaco Dormitator latifrons en La Isla, comunidad de Pechichal, parroquia de San Isidro, municipio de Sucre, provincia de Manabí, Ecuador.
The specimens were identified morphologically following the methodology of in Sabapathy-Allen (2019), and total DNA was extracted from about 20 specimens using the 'E.Z.N.A. Mollusk DNA Kit' (Omega Bio-Tek). Partial COI gene PCR products were obtained using the barcoding primer set LCO1490/HCO2198 (Folmer et al 1994) and the modified primers jgLCO1490/jgHCO2198 (Geller et al 2013), purified with the ExoSAP-It kit (Affimetrix) and sequenced using BigDye. v3.1 X terminator kit on ABI 3500 equipment (Thermo Fisher Scientific).
The resulting sequences were trimmed to remove primers. All sequences correspond to the same haplotype, which was compared to GenBank reference sequences using the BLASTN algorithm (Altschul et al 1990) to identify similarities. One sequence, representing the same haplotype from 20 individuals, was deposited in GenBank under the accession number PP716899.
A phylogenetic analysis was carried out to infer the lineage and possible origin of the samples, using as a basis the sequences published by Lee et al (2005), Gomes et al (2016), and Ludwig et al (2024), both about this species and others of the genus Corbicula, and the new genus available in Genbank (as of 04-30-2024) (n = 227). We selected one sequence per haplotype per country (Corbicula spp., n = 75; table 1s in supplementary material) with a length of 560 bp was selected. Phylogenetic analyses were performed following sequence alignment with Clustal. The total length of the analyzed matrix was 560 bp. The data were subjected to phylogenetic analysis using the maximum likelihood (ML) method. ML inference was performed using the PhyML program (Guindon and Gascuel 2003), available on the public web server Phylemon2 (http://phylemon.bioinfo.cipf.es). Statistical support for the resulting phylogenies was assessed by bootstrapping with 1,000 replicates (Felsenstein 1985). All trees were edited with FigTree software.
Tabla 1s. Secuencias del gen COI de Corbicula sp. utilizadas en el presente trabajo, con código de acceso Genbank y país de origen.
Results
The present findings represent the first report of C. fluminea for the province of Manabí, reaffirming its distribution and establishment in the river basins (table 3). We also report the first case in Ecuador of the presence of C. fluminea in an artificial culture system of the Pacific white shrimp Penaeus vannamei (Boone, 1931) and the Pacific fat sleeper fish Dormitator latifrons (Richardson, 1844).
Tabla 3. Lugares donde se han registrado ejemplares de Corbicula fluminea en Ecuador.
Among the sequences of C. fluminea available in Genbank, the Blast carried out revealed 100% similarity of the sequence obtained in Ecuador with other representatives, mainly from Europe (fig. 2; table 2s in supplementary material), Asia, and America (Argentina, Brazil, Peru, Ecuador, Mexico, Panama, Cuba and USA). In this study, four haplotypes were identified for the genus Corbicula in South America. The sequence obtained for Ecuador corresponds to the invasive lineage FW5 (form A/R).
Fig. 2. Corbicula spp. phylogenetic tree, based on the COI gene. The sequence from this study was aligned with other sequences from NCBI. Collapsed nodes are indicated by triangles. Values on the tree refer to bootstrap support. The number of sequences per node is shown in parentheses. Nodes with bootstrap values below 50 % were not included. Sequences from Ecuador are shown in red. Other sequences from South and Central America are in green. The text in light blue: sequences from these countries differ in one or two bases of the FW5 haplotype. Color boxes (groups according to Gomes et al (2016): pink: group 1; green: group 2; yellow: group 3; light blue: group 4). In group 3, only one sequence was used for South America (Argentina, Brazil and Colombia) since it is the same haplotype.
Fig. 2. Árbol filogenético de la Corbicula spp., basado en el gen COI. La secuencia de este estudio se ajustó a otras del National Center for Biotechnology Information (NCBI). Los nodos colapsados se indican con triángulos. Los valores en el árbol se refieren al soporte Bootstrap. Entre paréntesis, se indica el número de secuencias por nodo. Los nodos con valores Bootstrap inferiores al 50 % no se incluyeron. En rojo, se indican las secuencias de Ecuador. En verde, se indican otras secuencias de América del Sur y Central. En azul claro, se indican las secuencias de estos países que difieren en una o dos bases del haplotipo FW5. Los recuadros de color (grupos según Gomes et al (2016): rosa, grupo 1; verde: grupo 2; amarillo: grupo 3; azul claro: grupo 4). En el grupo 3, solo se utilizó una secuencia para América del Sur (Argentina, Brasil y Colombia), ya que se trata del mismo haplotipo.
Tabla 2s. Divergencia genética por pares (Kimura de dos parámetros, %) entre individuos de Corbicula p. evaluada empleando secuencias del gen COI.
Discussion
Corbicula fluminea is extensively distributed in South America (Darrigran et al 2020) and is found in several countries. In Ecuador, the species has been reported from the provinces of Esmeraldas, Santo Domingo de los Tsachilas, Los Ríos, and Guayas, with this record being the first report for the province of Manabí, and reaffirming its distribution and establishment in the river basins of Ecuador (table 3). Furthermore, it represents the first case of C. fluminea in an artificial culture system for the Pacific white shrimp, P. vannamei, and the Pacific fat sleeper D. latifrons.
The tree shows a topology similar to that of Lee et al (2005), Gomes et al (2016), and Ludwig et al (2024), with several clades with low support or unresolved, identifying four haplotypes for the genus in South America, three published by Lee et al (2005) and the new haplotype mentioned by Ludwig et al (2024) (FWBra, for Brazil).
The sequence obtained for Ecuador corresponds to the invasive lineage FW5 (form A/R), the most widely distributed lineage in America (Lee et al 2005, Gomes et al 2016, Ludwig et al 2024). It corresponds to the morphotype A/ R; and it has also been detected in Colombia (Ludwig et al 2024). The FW17 lineage (form C/S) has been detected outside the native distribution area, although it has not yet been reported from East Asia. In South America, it is found in Brazil, Colombia, and Argentina (Ludwig et al 2024).
The species C. fluminea presents several characteristics that indicate a high capacity to colonize different limnological environments, explaining its global distribution. Its life cycle favors the ability to invade other systems due to high growth rates, early maturation (Sousa et al 2008), and capacity for androgenesis and self- fertilization (Pigneur et al 2012), thus causing low genetic variability in their populations. The global phylogenetic analysis performed by Pigneur et al (2011) reveals that sexual lineages of Corbicula seem restricted to native areas, while androgenic reproduction is found both in native areas (Pigneur et al 2012) and in all invaded areas (Gomes et al 2016). Androgenic reproduction could have played an important role in the invasive success of Corbicula clams as androgenetic clams are generally hermaphroditic and capable of self-fertilization (Pigneur et al 2012).
In summary, androgenesis is the predominant reproductive mode within the hermaphrodite and invasive lineages of the genus Corbicula, with its ability to reproduce by cloning being a determining factor in its invasive success, having colonized American and European freshwater systems during the 20th century. However, in clams of Corbicula spp. androgenetic genetic mixing between different lineages has also occasionally been observed when the sperm of one lineage fertilizes the oocyte of another. Because of these occasional introgressions, the genetic relationships between Corbicula species remain unclear, and the biogeographic origins of invasive androgenetic lineages are difficult to identify. Despite this genetic mixture between invasive Corbicula lineages, genetic analyses place one of the invasive forms of Corbicula from South America as African (Vastrade et al 2022). However, as previously mentioned, a new COI haplotype (FWBra) was detected in a population from Brazil.
This report is the first to describe the presence of C. fluminea in an aquaculture production system with Pacific white shrimp in polyculture with the Pacific fat sleeper fish. Despite P. vannamei being a species of marine- estuarine origin, its adaptability to very low salinities allow adequate growth, and profitability can be greater when grown with D. latifrons. These production systems have low salinity (2-5‰, JJ Bernal-Zambrano), which allows the existence and proliferation of C. fluminea. Despite being a freshwater species, C. fluminea can tolerate salinities of up to 10-14 ‰ (McMahon 2000), allowing it to colonize upstream areas of estuaries (Franco et al 2012, Ilarri et al 2014) where a high number of shrimp farms are established in Ecuador. Although there is no apparent adverse effect on performance with the presence of C. fluminea, this species is one of those that have a higher filtration rate than other freshwater filter-feeding mollusks (McMahon 1991), Therefore some of the first impacts that it could cause on production systems would be the decrease in phytoplankton load, and the imbalance in alkalinity, calcium and other essential minerals in the crop, affecting the balance of the system. Furthermore, the consequent water clearing that occurs due to the filtration produced by C. fluminea may increase predation by birds (Aldridge et al 2008, Lodeiros and Torres 2018, Lodeiros et al 2019).
Given the potential threat of the invasive species C. fluminea, it is crucial to monitor aquaculture systems to prevent its establishment. In systems already invaded by this species, it is equally important to establish the possible effect on said systems and surrounding ecosystems.
Acknowledgements
Partial financial support was received by GD-DEGG from Agencia Nacional de Promoción Científica y Tecnológica (PICT-2019-01417); GD-DEGG from Universidad Nacional de La Plata (UNLP 11/N927); DEGG-GD from Consejo Nacional de Investigaciones Científicas y Técnicas (PIP 1966) and CL from Invasive mollusk species (exotic and native) in shrimp farming systems in Ecuador Project. This work is part of the research carried out by the eMIAS (South American Alien Molluscs Specialist Group, emiasgroup.wixsite.com/emias) of which CL, GD and DEGG are members
