Introduction
The family Ostreidae Rafinesque, 1815 encompasses a diverse group of sessile bivalves widely distributed in tropical, subtropical, and temperate coastal environments, typically to depths up to 30 m (Mikkelsen and Bieler, Reference Mikkelsen and Bieler2008). Members of this family attach to natural or artificial hard substrates, often forming dense aggregations or biogenic reefs that play crucial roles as ecosystem engineers. These reef structures enhance habitat complexity, modulate hydrodynamic energy, and support high biodiversity by providing refuge and substrate for associated fauna (Baggett et al., Reference Baggett, Powers, Brumbaugh, Coen, DeAngelis, Greene, Hancock and Morlock2014).
The scientific and economic interest in oysters lies in their dual value: on one hand, they are key species for artisanal fisheries and aquaculture; on the other, they serve as sensitive indicators of environmental change due to their bioaccumulation capacity and tolerance to fluctuations in salinity, temperature, and pollution.
Globally, Ostreidae includes 15 genera within 4 subfamilies (MolluscaBase, 2026). In the Colombian Caribbean, six species have been recorded across four genera: Ostrea equestris Say, 1834, Ostrea sp., Crassostrea rhizophorae (Guilding, 1828), Crassostrea virginica (Gmelin, 1791), Hyotissa hyotis (Linnaeus, 1758), and Dendostrea (sometimes as Lopha or Ostrea) frons (Linnaeus, 1758) (Cosel, Reference Cosel1986; Díaz and Puyana, Reference Díaz and Puyana1994; Yidi-Daccarett and Sarmiento-Bossio, Reference Yidi-Daccarett and Sarmiento-Bossio2011). These oysters occur on mangrove roots, rocky and coral substrates, and are increasingly found on anthropogenic structures such as pilings, marina facilities, and port walls.
In Colombia, studies on Ostreidae in the Caribbean have been focused on taxonomy and population dynamics (e.g. Reyes and Campos, Reference Reyes and Campos1992; Mancera and Mendo, Reference Mancera and Mendo1996; López-Sánchez and Mancera-Pineda, Reference López-Sánchez and Mancera-Pineda2019), contamination (e.g. Escobar-Nieves, Reference Escobar-Nieves1988; Campos, Reference Campos1990; López et al., Reference López, Manjarrez, Herrera, Montes, Olascuaga and Ortega2010), and farming and repopulation (e.g. Wedler, Reference Wedler1983; Cáez and Vélez, Reference Cáez and Vélez2000; Velasco and Barros, Reference Velasco, Barros, Lovatelli, Farías and Uriarte2008; Velasco et al., Reference Velasco, Vega, Acosta and Barros2010). Notably, these studies consistently report only C. rhizophorae as the representative oyster species in the region. According to Merino et al. (Reference Merino, Bonilla and Bages2013), this oyster has been sporadically cultivated along the Colombian Caribbean coast, showing favourable results in terms of both quality and growth. Nevertheless, commercialization has posed significant challenges for producers, which explains the absence of active farming initiatives at present. Despite their ecological and economic importance, taxonomic resolution remains limited due to high intraspecific morphological variability and historical synonymizations, particularly between C. rhizophorae and C. virginica. Moreover, little is known about their genetic diversity, habitat degradation responses, and vulnerability to anthropogenic pressures.
Oysters are well known for their invasive potential, driven by broad environmental tolerance, rapid growth, and geographical transfer via aquaculture and maritime transport. Several global examples illustrate this pattern: C. virginica has been widely translocated beyond its native range; Magallana gigas (Thunberg, 1793) is one of the most successful marine invaders, introduced to over 50 countries (Fofonoff et al., Reference Fofonoff, Ruiz, Steves, Simkanin and Carlton2018); and species such as H. hyotis and O. stentina Payraudeau, 1826 have been recently reported outside their native distributions (Bieler et al., Reference Bieler, Mikkelsen, Lee and Foighil2004; Papadopoulos et al., Reference Papadopoulos, Giantsis, Lattos, Triantafyllidis and Michaelidis2024), often associated with artificial substrates. Together, these cases highlight the role of human-mediated transport in facilitating oyster invasions and their capacity to alter benthic communities.
Recent studies have shown that morphological characters alone are insufficient to delimit oyster species, highlighting the need for an integrative taxonomic approach (Ferreira et al., Reference Ferreira, Legat, Lazoski, Freire, Cham and Melo2023) that combines taxonomic, ecological, and molecular data. In this context, the present study aims to improve the understanding of ostreid diversity in the central Colombian Caribbean by analysing oysters from two contrasting environments, the Puerto Velero marina (PVm) and the Mallorquín Coastal Lagoon (MCL). We apply an integrative taxonomic framework to resolve the identity of key oyster taxa occurring on both natural and artificial substrates, with particular attention to the detection of non-native species and their potential ecological implications.
Materials and methods
Study area
The Atlántico Department is in the central Colombian Caribbean (see Figure 1) and spans approximately 71 km of coastline (Posada and Henao, Reference Posada and Henao2008). The region exhibits a tropical seasonal climate, characterized by three distinct periods: a dry season with strong northeasterly winds from December to April, a transitional period from May to July, and a rainy season from August to November (Pujos et al., Reference Pujos, Pagliardini, Steer, Vernette and Weber1986; Andrade-Amaya, Reference Andrade-Amaya2001). This coastal zone is heavily influenced by the discharge of the Magdalena River, the largest fluvial system in Colombia, which delivers an estimated 142.6 × 106 tons of suspended sediments annually into the Caribbean Sea (Restrepo et al., Reference Restrepo, Orejarena and Torregroza2017). This sediment influx leads to low water transparency and drives dynamic coastal geomorphological processes.
Occurrence of Crassostrea virginica and Saccostrea lineage F in Colombia. Records from the Atlántico Department include the Mallorquín Coastal Lagoon (MCL) and Puerto Velero Marina (PVm). In MCL, the stations from which material was analysed for DNA barcoding are indicated as follows: Punta Felix – P5; Dock – P6; Punta Saco – P7; Old Garbage Dump – P8. In the panel on the right, records of Saccostrea lineage F from Central and South America are indicated, including occurrences in Panamá (Pagenkopp-Lohan et al., Reference Pagenkopp-Lohan, Hill-Spanik, Torchin, Strong, Fleischer and Ruiz2015), Colombia (present study), and Brazil (Galvão et al., Reference Galvão, Alves and Hilsdorf2017; Do Amaral et al., Reference Do Amaral, Simone, Tâmega, Barbieri, Calazans, Coutinho and Spotorno-Oliveira2020). Likewise, the distribution ranges of Crassostrea rhizophorae and C. virginica are shown based on molecular records available in GenBank. MRD, Magdalena River Delta.
Figure 1 Long description
The map shows the distribution of Crassostrea rhizophorae, Crassostrea virginica and Saccostrea lineage F in Colombia and surrounding regions. The main map highlights Colombia with specific focus on the Atlántico Department, showing locations like Mallorquín Coastal Lagoon (MCL) and Puerto Velero Marina (PVm). An inset map provides a detailed view of these sites, with stations P5, P6, P7 and P8 marked in MCL. Another inset map shows the distribution of the species along the coasts of North, Central and South America, with Crassostrea rhizophorae in green, Crassostrea virginica in blue and Saccostrea lineage F in red. The map includes a compass rose and scale bar for reference.
One prominent feature shaped by these dynamics is the Puerto Velero sandspit, formed by sediment accumulation enhanced by the construction of breakwaters at Bocas de Ceniza (Restrepo et al., Reference Restrepo, Zapata, Díaz, Garzón-Ferreira and García2006; Anfuso et al., Reference Anfuso, Rangel-Buitrago, Correa, Randazzo, Jackson and Cooper2015). On the sheltered side of this sandspit lies the PVm (10°56′37.89″ N, 75°2′26.94″ W) (Figure 1), a small-to-medium facility primarily serving recreational vessels, including those transiting from the United States and Europe. The marina comprises artificial structures that provide abundant hard substrates, favouring the establishment of sessile invertebrates such as oysters.
In contrast, the MCL is a shallow brackish water body located on the northeastern margin of the Atlántico Department (11°02′20.39″N, 74°50′53.91″W) (Figure 1), covering approximately 830 hectares with an average depth of 1 m (CRA, 2021a). It connects with the Caribbean Sea to the north through a natural inlet and with the Magdalena River to the east via three box culverts, allowing periodic freshwater input depending on hydrological conditions (CRA, 2021b). This hydrological connectivity generates pronounced spatial and temporal variability in physical and chemical parameters. Average salinity is reported at 16.4 psu, with fluctuations between 5.8 and 22 psu depending on the sector (CRA, 2018); however, salinities up to 29–30 psu were recorded in January and July 2025 (this study). Water temperature ranges between 27.6°C and 31.9°C throughout the year (CRA, 2021b).
The lagoon is bordered by mangrove vegetation, which is composed of four species. Avicennia germinans (L.) L. is the most common taxon, followed by Laguncularia racemosa (L.) C.F. Gaertn. and Rhizophora mangle L., while Conocarpus erectus L. occurs less frequently (MinAmbiente, 2016). These mangrove systems provide essential substrate for benthic communities and contribute to the lagoon’s productivity and ecological heterogeneity.
Study sites and field sampling
Field trips were made in the PVm, examining the artificial structures associated with the main dock. The oysters were found on metal pilings in the shallowest part of the marina (approximately 0–30 cm deep). In MCL, four sampling stations (Punta Felix – P5, Dock – P6, Punta Saco – P7, Old Garbage Dump – P8) (Figure 1) were established around the lagoon to assess the presence of the species on the mangrove roots. Field surveys were conducted during the second half of 2024. The oyster specimens were collected using a chisel, and all specimens were preserved in 96% ethanol for morphological and molecular analysis.
Morphological identification
Initial identification to the lowest possible taxonomic level was performed using morphological and anatomical criteria following Cosel (Reference Cosel1986), Mikkelsen and Bieler (Reference Mikkelsen and Bieler2008), and Do Amaral and Simone (Reference Do Amaral and Simone2014, Reference Do Amaral and Simone2016). Diagnostic characters assessed included shell shape and sculpture, hinge morphology, the presence of chomata, mantle tentacle shape and coloration, and adductor muscle scar patterns. All voucher specimens were deposited in the Museo de Historia Natural Marina de Colombia – Makuriwa (MHNMC), INVEMAR, Santa Marta, under collection acronym INV MOL.
DNA extraction, PCR amplification, and sequencing
Ten specimens were selected for molecular analysis: six assigned to Crassostrea and four to Saccostrea. Soft tissue (mantle and adductor muscle) was dissected and sampled separately from each individual. Genomic DNA was isolated using the CorpoGen DNA2000 kit and amplification of the mitochondrial COI gene was carried out using the 5X Hot FirePol Blend Master Mix to Load RTL and the universal COI primers LCO1490 (5′-GGTCAACAAATCATAAAGATATTGG-3′) and HC02198 (5′-TAAACTTCAGGGTGACCAAAAAATCA-3′) (Folmer et al., Reference Folmer, Black, Hoeh, Lutz and Vrijenhoek1994), obtaining a COI fragment of ∼700 bp. Annealing conditions of 50°C were used for COI, and thermal protocols included the following steps: an initial 10 min denaturation at 95°C, then 30 s at 94°C, 30 s annealing step, and 60 s at 72°C, for 35 cycles, and a final 5 min extension at 72°C. Amplified products were sequenced using the Sanger method with both strands (sequenced by CorpoGen Corporation – Colombia).
Phylogenetic analysis methods
Forward and reverse sequences were assembled and edited using Geneious Prime version 2023.0.4 (Kearse et al., Reference Kearse, Moir, Wilson, Stones-havas, Cheung, Sturrock, Buxton, Cooper, Markowitz, Duran, Thierer, Ashton, Meintjes and Drummond2012) and compared against the nucleotide database of GenBank to confirm the successful amplification of the target marker/organism. The sequences generated in this work were deposited in GenBank under the accession numbers PZ324985–PZ324999. These new DNA sequences were combined and analysed with sequences provided by Pagenkopp-Lohan et al. (Reference Pagenkopp-Lohan, Hill-Spanik, Torchin, Strong, Fleischer and Ruiz2015), Galvão et al. (Reference Galvão, Alves and Hilsdorf2017), and additional sequences from GenBank for the COI marker of selected taxa within the family Ostreidae. Members of the genus Ostrea and Dendostrea were used as outgroups (Supplementary Material 1).
Sequences were aligned in MAFFT v7.53 with L-INS-I algorithm and ‘–maxiterate 1000’ option (Katoh et al., Reference Katoh, Asimenos and Toh2009). Maximum likelihood (ML) reconstruction was performed in IQ-TREE2 (Minh et al., Reference Minh, Schmidt, Chernomor, Schrempf, Woodhams, Von Haeseler and Lanfear2020), and we analysed using ModelFinder (Kalyaanamoorthy et al., Reference Kalyaanamoorthy, Minh, Wong, Von Haeseler and Jermiin2017) for the best-fitting evolutionary model according to the best Bayesian Information Criterion score: HKY + F + I + R3. We assessed branch support with 1000 Shimodaira-Hasegawa (SH)-like approximate likelihood ratio test (SH-aLRT) (Guindon et al., Reference Guindon, Dufayard, Lefort, Anisimova, Hordijk and Gascuel2010), 1000 ultrafast bootstrap (UFBoot2, uBS) replicates (Hoang et al., Reference Hoang, Chernomor, Von Haeseler, Minh and Vinh2018), parametric aLRT (Anisimova and Gascuel, Reference Anisimova and Gascuel2006), and approximate Bayes tests (aBayes) (Anisimova et al., Reference Anisimova, Gil, Dufayard, Dessimoz and Gascuel2011). The resulting trees were edited and illustrated using TreeGraph v2 (Stöver and Müller, Reference Stöver and Müller2010).
Examination of museum material
To evaluate the historical representation of Ostreidae in the region, in April 2026, material deposited in the MHNMC was reviewed from different localities along the Caribbean coast of Colombia. The revision included the examination of both catalogued and some uncatalogued lots, together with their associated collection data. This information is available through the digital data repositories of the MHNMC database and the GBIF web platform (https://www.gbif.org/dataset/efd53c28-ca18-4eca-803e-4dc39facbaf1).
Results
Of the oyster species examined in this study, C. virginica was found only at very low densities in the MCL, based on the field examination of individuals with the shape of Crassostrea (large, elongated, and triangular/pear-shaped). The presence of Saccostrea lineage F (name according to Lam and Morton, Reference Lam and Morton2006; Sekino and Yamashita, Reference Sekino and Yamashita2016; Duangdee et al., Reference Duangdee, Sanpanich, Lukehurst and Wells2025; Tan et al., Reference Tan, Wells, Tan, Lukehurst, Morgan and Fotedar2025) was confirmed in the Atlántico Department, with specimens recorded at both localities (PVm and MCL). At the time of sampling, surface salinity was recorded at an average of 26.5 psu in the MCL and 28.3 psu in PVm.
Class Bivalvia Linnaeus, 1758
Family Ostreidae Rafinesque, 1815
Genus Crassostrea Sacco, 1897
Crassostrea virginica (Gmelin, 1791) (Figure 2a–m)
Crassostrea virginica. (a) Right valve, outer side, INV MOL12867, showing polychaete boring tunnels and sponges growing in patches. (b) Right valve, inner side, INV MOL12867, showing the oval and purple adductor muscle scar. (c) Arrangement of the tentacles on the edge of the mantle INV MOL12865. (d) Oysters attached to mangrove roots in the Mallorquín Coastal Lagoon. (e) Inner cavities of boring polychaetes in the right valve INV MOL12866. (f, g) INV MOL12861, (f) right valve, outer side; (g) right valve, inner side. (h, i) INV MOL12865, (h) left valve, outer side; (i) right valve, inner side. (j, k) INV MOL12868, (j) right valve, outer side; (k) right valve, inner side. (l, m) INV MOL12869, (l) right valve, outer side; (m) right valve, inner side. Scale bars: a–b, e–m, 2 cm; c, 0.5 mm.
Examined material with molecular support: INV MOL12861, 1 individual (26/10/2024, P7, MCL); INV MOL12865, 1 individual (26/10/2024, P8, MCL); INV MOL12866, 1 individual (26/10/2024, P5, MCL); INV MOL12867, 1 individual (26/10/2024, P8, MCL); INV MOL12868, 1 individual (26/10/2024, P8, MCL); INV MOL12869, 1 individual (26/10/2024, P8, MCL).
Diagnosis: Shells elongate, thick, reaching up to 113.4 mm in length (mean: 82.4 ± 25.9 mm × 43.2 ± 8.4 mm, n = 6). External coloration beige to white with brown/purple blotches (Figure 2a). External surface with outer undulations and layered lamellae. Left valve deeply cupped; umbonal region pronounced. Interior white with pigmented margin, lacking chomata; adductor muscle scar purple, oval, located posteroventrally (Figure 2b). Outer mantle fold lacking tentacles; middle fold with short tentacles of variable shape; inner fold with longer tentacles uniformly distributed (Figure 2c). See Do Amaral and Simone (Reference Do Amaral and Simone2014) for additional morphological details.
Ecology: In the MCL, individuals displaying the typical Crassostrea-like shell morphology were found only at low densities attached to mangrove roots of L. racemosa, R. mangle (Figure 2d), and concrete debris. The shells of C. virginica were highly affected by shell-boring spionid polychaetes, with boring tunnels on both the exterior and interior sides of the shell (Figure 2a, e). Polychaetes from the genus Syllis and nematodes were also found living in the empty tunnels left in the exterior side of the oyster valves. Additionally, juvenile anemones, barnacles, sponges, bryozoans, and algae were found covering the oysters.
Geographic distribution: Western Atlantic: Canada, USA, Mexico, Panama, Venezuela, West Indies (Stanley and Sellers, Reference Stanley and Sellers1986; Pagenkopp-Lohan et al., Reference Pagenkopp-Lohan, Hill-Spanik, Torchin, Strong, Fleischer and Ruiz2015), Colombia (this study).
Remarks: Despite the diagnosis described above, important diagnostic characters such as the shell shape (Figure 2a, b, f–m), the presence of outer undulations, the deepness of the umbonal cavity, and the shape of the mantle tentacles were observed to be variable, without the possibility of establishing a general diagnosis applicable to all the specimens. Given that the only way to accurately differentiate this species and C. rhizophorae is through DNA analysis (Ferreira et al., Reference Ferreira, Legat, Lazoski, Freire, Cham and Melo2023), the examined material listed above shows only the individuals with molecular support, although these were not the only specimens found and collected during this study.
Subfamily Saccostreinae Salvi and Mariottini, 2016
Genus Saccostrea Dollfus and Dautzenberg, 1920
Saccostrea lineage F (Figure 3a–f)
Saccostrea lineage F INV MOL12864. (a) Complete individual, showing the right valve; next to the dissected oyster is another unopened individual attached. (b) Right valve. (c) Detail of chomata along the inner margin. (d) Adductor muscle scar. (e) Pattern of the tentacles on the edge of the mantle. (f) Field observation of oysters in the Puerto Velero Marina, including individuals colonizing artificial substrates (metallic pilings). Scale bars: a, b, 1 cm; c, d, 3 mm; E, 1 mm; f, metal piling perimeter 87 cm.
Examined material with molecular support: INV MOL12862, oyster cluster (28/09/2024, PVm); INV MOL12863, oyster cluster with 4 individuals (27/06/2024, PVm); INV MOL12864, 1 individual (26/10/2024, P6, MCL); INV MOL12888, 1 individual (05/12/2024, PVm).
Diagnosis: Shell thick and solid, pear-shaped, with an undulated outline. Specimens smaller than typical literature descriptions (mean: 32.0 ± 4.1 mm × 21.3 ± 5.8 mm, n = 4) (Figure 3a, b). Right valve moderately flattened with prominent chomata along the inner margin (Figure 3c). Left valve larger and deeply cupped. Shell margin strongly undulating or scalloped; umbonal cavity deep. Interior white to yellowish with slight purplish tint and diffuse darker patches. Adductor muscle scar small, oval or slightly reniform, yellowish-brown with paler crescent-shaped bands (Figure 3d). Mantle tentacles elongated, yellow with dark patches (Figure 3e).
Ecology: Clusters of Saccostrea oysters were found attached to mangrove roots in MCL and artificial substrata such as metal pilings and concrete slabs at PVm, at depths of no more than 0.5 m (Figure 3f). In the MCL, the individuals were found forming clusters with other bivalve species such as Isognomon sp. and Mytella strigata (Hanley, 1843).
Geographic distribution: Australia (McDougall et al., Reference McDougall, Nenadic, Richardson and Healy2024), Taiwan, China, Singapore (Lam and Morton, Reference Lam and Morton2006), Panama (Pagenkopp-Lohan et al., Reference Pagenkopp-Lohan, Hill-Spanik, Torchin, Strong, Fleischer and Ruiz2015), Japan (Sekino and Yamashita, Reference Sekino and Yamashita2016), Brazil (Galvão et al., Reference Galvão, Alves and Hilsdorf2017), Thailand (Duangdee et al., Reference Duangdee, Sanpanich, Lukehurst and Wells2025).
Remarks: During field examination, young specimens of C. virginica can be confused with Saccostrea lineage F, given that the typically outer undulations on the shell of C. virginica can be interpreted as the ornamentation in the shell edges of Saccostrea lineage F (Figure 2f, g). To correctly differentiate both genera, the presence or absence of chomata, the shape of the adductor muscle, and the shape and coloration of the mantle tentacles should be assessed.
Molecular analyses of Crassostrea and Saccostrea
The ML phylogenetic reconstruction of the Ostreidae (Figure 4), based on COI sequences (aligned length: 1,732 bp), recovered well-supported clades for the analysed taxa. All six specimens of C. virginica clustered with conspecific sequences from Canada, Cuba, Mexico, Panama, and the Atlantic coast of the United States, with consistently high support across all metrics (99.8/1/1/99).
Phylogenetic reconstruction based on maximum likelihood analysis of Crassostrea virginica and Saccostrea lineage F within the family Ostreidae using COI. Each node corresponds to a specimen, identified by its sampling locality and GenBank accession number. Support values with SH-aLRT support (%)/parametric aLRT support/aBayes support/ultrafast bootstrap support (%).
Figure 4 Long description
The phylogenetic tree is oriented vertically, depicting evolutionary relationships within the Ostreidae family based on COI sequences. Each node represents a specimen identified by its sampling locality and GenBank accession number. The tree includes support values for SH-aLRT, parametric aLRT, aBayes and ultrafast bootstrap, displayed at each node. The tree is color-coded, with different clades highlighted in blue, red and green. The blue clade includes various Saccostrea species, while the red clade features Crassostrea virginica specimens from multiple locations, including Canada, Cuba, Mexico, Panama and the Atlantic coast of the United States. The green clade includes Ostrea species. Branch lengths and support values are indicated, showing the evolutionary distances and confidence levels for each relationship. The tree provides a detailed view of the genetic diversity within the Ostreidae family.
In contrast, the four specimens identified as Saccostrea lineage F formed a strongly supported clade (96.7/1/1/99) together with sequences attributed to S. cuccullata from Australia and Japan, S. malabonensis (Faustino, 1932) from China and Myanmar, and Saccostrea sp. from Panama and clearly differ from the sequence of the specimen found in the type locality, Ascension Island (Atlantic Ocean), as S. cuccullata sensu stricto. This clade was also recovered as a sister group to the specimens from Bertioga, São Paulo State, Brazil, also with maximal support (99.9/1/1/100).
Ostreidae MHNMC
Material deposited in the MHNMC was reviewed in order to evaluate the historical representation of Ostreidae in the region, assessing lots from several localities along the Caribbean coast of Colombia, including: Manaure and offshore gas platforms in La Guajira Department; Punta Betín, the Ciénaga Grande de Santa Marta (CGSM) and Chengue in the Magdalena Department; the Cartagena Bay and Tintipán Island in the Bolívar Department; and the Gulf of Morrosquillo (Sucre Department). Most specimens consisted of dry shells, limiting the evaluation of diagnostic anatomical characters. The available information was not conclusive for species-level identification in several cases.
Representatives of Dendostrea frons were identified in lots INV MOL262, INV MOL7815, INV MOL7819, INV MOL7827–7829, and INV MOL7831–7832. Material catalogued as Ostrea equestris (INV MOL240, INV MOL9998-9999, INV MOL10001–10002, INV MOL10004–10010, INV MOL10013–10014) was also examined; however, lot INV MOL240 corresponds to Hyotissa sp., whereas the remaining lots correspond to Crassostrea sp., as none of the examined specimens presented chomata.
The remaining material (INV MOL195, INV MOL233, INV MOL239, INV MOL520, INV MOL789, INV MOL826–843, INV MOL846–848, INV MOL1029) is catalogued as C. rhizophorae, and only three lots are identified as C. virginica. Two lots from Tintipán Island (uncatalogued lot CIS-098) and Cartagena Bay (INV MOL10008) may potentially correspond to Saccostrea according to our criteria; nevertheless, further studies are required.
The material deposited in the mollusc collection of the MHNMC represents an important historical reference for understanding the oyster species present in the region over several decades, from the 1960s through the 1990s, which could be interpreted as part of the native assemblage, considering that invasive species, particularly those of Saccostrea, have only been reported in the Caribbean in recent decades. Unfortunately, no reference material associated with the studies of Cosel (Reference Cosel1986), who revised the oysters from the CGSM, the largest and most important lagoon complex in the Colombian Caribbean, was found in the collection. However, other material from those decades associated with attempts to cultivate Crassostrea on different substrates was available and reviewed, revealing that shell morphology varied according to culture conditions, particularly between bottom-grown and suspended oysters. Although most of the material lacked soft tissues, traces of tissue were detected in some shells, which may allow future molecular studies for the identification of this material. In the case of Crassostrea, the collection labels and associated catalogue information were useful primarily for assigning specimens to the genus level, rather than for reliably confirming species identities.
Discussion
Within the Colombian Caribbean, the species historically reported as C. rhizophorae is strongly associated with R. mangle root systems (Reyes and Campos, Reference Reyes and Campos1992) and has long been recognized as the dominant, or most frequently recorded, oyster species in scientific surveys. At Punta Roca (northern Atlántico Department), shell accumulations likely from the Magdalena River estuarine system were initially identified as C. rhizophorae based on shell morphology (Gracia et al., Reference Gracia, Pacheco-Medina, Paternina-Ramos, Peña-Granados and Rangel-Buitrago2024). However, molecular studies indicate that C. rhizophorae coexists with the similar C. virginica in the southern Caribbean (Pagenkopp-Lohan et al., Reference Pagenkopp-Lohan, Hill-Spanik, Torchin, Strong, Fleischer and Ruiz2015), and due to their limited morphological differentiation (Ferreira et al., Reference Ferreira, Legat, Lazoski, Freire, Cham and Melo2023, Reference Ferreira, Gomes, Freire, Scaranto, Zacchi and Melo2025), the identity of previous records in the area remains uncertain.
Meanwhile, C. virginica (Gmelin, 1791), another native Western Atlantic oyster, is a larger species distributed from North America to the Caribbean that supports a major oyster industry. It commonly inhabits estuaries and behind barrier islands, where it may form extensive intertidal and subtidal reefs on firm substrates (Stanley and Sellers, Reference Stanley and Sellers1986; Carriker and Gaffney, Reference Carriker, Gaffney, Kennedy, Newell and Eble1996). Given that C. virginica was historically considered synonymous with C. rhizophorae, the identity of many regional records remains uncertain. However, for nearly two decades, Mikkelsen and Bieler (Reference Mikkelsen and Bieler2008), Pagenkopp-Lohan et al. (Reference Pagenkopp-Lohan, Hill-Spanik, Torchin, Strong, Fleischer and Ruiz2015), MolluscaBase eds (2026), and other studies have recognized both oysters as valid species.
In the MCL, local fishermen report that Crassostrea species have not been observed for approximately 5 years, although they were previously harvested for consumption (pers. comm. 2024–2025). Their historical presence in the lagoon is, therefore, well supported. Crassostrea rhizophorae was reported by INVEMAR (2005) during an assessment of mangrove ecosystems in the Atlántico Department, and experimental studies on reproductive biology using specimens from MCL were conducted by Wedler (Reference Wedler1983), Cáez and Vélez (Reference Cáez and Vélez2000), and Velasco et al. (Reference Velasco, Vega, Acosta and Barros2010). Consequently, it is unclear whether C. virginica and/or C. rhizophorae have historically occurred in MCL, whether C. virginica has replaced a previously established population of C. rhizophorae, or whether C. rhizophorae persists but remains undetected due to its morphological similarity to Saccostrea or other ostreids. Notably, shells with the typical morphology of Crassostrea are currently rare in the lagoon; only a few individuals were observed, corresponding to those analysed here as C. virginica. The absence of historical reference material further limits the reconstruction of past population dynamics.
Crassostrea rhizophorae, as referred to in the literature, is a species that historically formed extensive natural oyster banks and was once intensively harvested in the CGSM, an estuarine–barrier island complex that extends northward towards the MCL. Its decline, driven mainly by sedimentation, led to the loss of a critical habitat, oyster reefs, and triggered a restructuring of the benthic community (Viloria-Maestre et al., Reference Viloria-Maestre, Acero and Blanco2012). A key element in this process was the dreissenid bivalve Mytilopsis sallei (Récluz, 1849), which thrived on oyster banks at densities of up to 5,000 ind./m2 and constituted the principal prey of the striped mojarra Eugerres plumieri (Cuvier, 1830) (Viloria-Maestre et al., Reference Viloria-Maestre, Acero and Blanco2012). The burial of oyster reefs by sediments from Sierra Nevada tributaries and, subsequently, from the Magdalena River, caused the disappearance of M. sallei, depriving mojarras of their main food source and precipitating a cascade of ecological effects that reduced the lagoon’s carrying capacity (Viloria-Maestre et al., Reference Viloria-Maestre, Acero and Blanco2012).
Historical analyses of the malacofauna conducted in 2005 in the CGSM suggested that, at that time, environmental conditions could support only a limited number of mollusc species, mainly restricted to sectors near Boca de La Barra where marine influence persisted, particularly during the dry season (Millán, Reference Millán2005). According to that study, much of the lagoon was characterized by elevated sedimentation, altered salinity, limited substrate availability, and reduced food resources, conditions interpreted as unfavourable for several species that had previously formed dense populations, as documented by Cosel (Reference Cosel1986) and Palacio (1983 in Millán, Reference Millán2005). Notably, C. rhizophorae, formerly considered widespread and abundant in the system, was not recorded as part of the living community during those surveys. Instead, Millán (Reference Millán2005) reported mainly thanatocoenoses composed of degraded shells, interpreted as evidence of substantial historical changes in the malacofauna of the lagoon.
A similar process may currently be occurring in the MCL, which has undergone intense sedimentation in recent decades, resulting in the loss of depth and habitat. Signs of this process include benthic organisms, such as sponges, being partially buried by sediments (Paternina-Ramos et al., Reference Paternina-Ramos, Gracia, Pacheco-Medina, Gutiérrez and Zea2026). It should be emphasized that the search for Crassostrea along the coastline of the Department and in the MCL yielded no significant results. No specimens were observed in their main habitat, the mangrove roots in MCL, where Saccostrea and other bivalves predominated. Only a few of the specimens used for molecular analysis were found on rocks or concrete debris in an area adjacent to urban settlements (Old Garbage Dump – station P8). These individuals were recognized and collected because they exhibited the typical Crassostrea shell form, i.e. elongated oval and solid valves.
Direct references to C. virginica in Colombia include the photograph published by Yidi-Daccarett and Sarmiento-Bossio (Reference Yidi-Daccarett and Sarmiento-Bossio2011), based on material collected in Cartagena (10°18.413′ N, 75°30.687′ W; depth: 0 m) in the central-western sector of the Colombian Caribbean; 4 valves of the INV MOL239 lot from Manaure, La Guajira (North of the Colombian Caribbean), collected in 1983; 15 valves of the lot INV MOL10015; and 3 valves in INV MOL10016, the last both from a port area in Cartagena collected in 2010 (Suárez-Mozo, Reference Suárez-Mozo2011 – unpublished data). The first lot (INV MOL239) was initially identified by R. Kaufmann in 1965 as C. virginica but was subsequently reassigned to C. rhizophorae. Nonetheless, Cosel (Reference Cosel1986) and Díaz and Puyana (Reference Díaz and Puyana1994) noted the variability of C. rhizophorae and suggested that it might represent an ecological form of C. virginica. Based on the evidence available at the time, however, they did not support the recognition of C. virginica, which indicates that, over time and across studies in the Colombian Caribbean, both species may have been treated as a single taxon.
In recent years, representatives of the exotic genus Saccostrea have been reported in Panamá and Brazil (Pagenkopp-Lohan et al., Reference Pagenkopp-Lohan, Hill-Spanik, Torchin, Strong, Fleischer and Ruiz2015; Galvão et al., Reference Galvão, Alves and Hilsdorf2017; Do Amaral et al., Reference Do Amaral, Simone, Tâmega, Barbieri, Calazans, Coutinho and Spotorno-Oliveira2020). In Panama, individuals were abundant and commonly found attached to mangrove rhizophores, closely associated with C. rhizophorae (Pagenkopp-Lohan et al., Reference Pagenkopp-Lohan, Hill-Spanik, Torchin, Strong, Fleischer and Ruiz2015). Similarly, in Brazil, specimens were found attached to mangrove roots, rocky shores, stones, and gravel, in the riverbed, forming clusters of 10–20 individuals and coexisting with native oyster species such as Crassostrea spp. and Ostrea sp. (Galvão et al., Reference Galvão, Alves and Hilsdorf2017). In the port environments of Santa Marta (Colombia), Moncaleano-Niño et al. (Reference Moncaleano-Niño, Barrios-Latorre, Poloche-Hernández, Becquet, Huet, Villamil, Thomas-Guyon, Ahrens and Luna-Acosta2017, Reference Moncaleano-Niño, Luna-Acosta, Gómez-Cubillos, Villamil and Ahrens2018) also recorded this genus in experimental studies, although its identity was not clarified. The genus Saccostrea, currently the only genus in the subfamily Saccostreinae, with at least 12 recognized species (MolluscaBase, 2026), is widely distributed in tropical and subtropical regions of the Indo-Pacific and is not native to the Caribbean; its occurrence in the region raises important questions about potential introduction pathways and mechanisms of dispersal. The material collected from both artificial and natural substrates in this study provides clear evidence of its presence in the Colombian Caribbean.
The Saccostrea species delimitation is problematic due to high morphological variability and overlapping distributions. Lam and Morton (Reference Lam and Morton2006), Sekino and Yamashita (Reference Sekino and Yamashita2016), and McDougall et al. (Reference McDougall, Nenadic, Richardson and Healy2024) showed that this group is a complex of multiple genetic lineages, highlighting the need for integrative taxonomy (morphology + DNA) to accurately resolve their identities. According to Tan et al. (Reference Tan, Wells, Tan, Lukehurst, Morgan and Fotedar2025), Saccostrea cuccullata sensu stricto, once thought to include western Atlantic populations, is in fact restricted to the central-south Atlantic, including the West African coast. DNA data from the type locality (Ascension Island) demonstrate that it is genetically distinct from other lineages, indicating that many records historically assigned to S. cuccullata actually represent different cryptic species.
In this context, several genetic lineages have been recognized, with lineage F encompassing material from the western Atlantic. The identity of this lineage remains unresolved despite molecular evidence (16S rRNA) supporting it as a distinct genetic clade. In the literature, lineage F has been associated with different nominal taxa, particularly S. malabonensis , based on its generally small size, cupped left valve, and narrow attachment area, and it has also been noted to resemble S. circumsuta (A. A. Gould, 1850) in some shell traits (Sekino and Yamashita, Reference Sekino and Yamashita2016). Additionally, previous studies have placed it within the broader S. cuccullata complex, further complicating its interpretation. More recently, Duangdee et al. (Reference Duangdee, Sanpanich, Lukehurst and Wells2025) showed that sequences previously attributed to S. forskahlii (currently listed as Ostrea forskahlii Gmelin, 1791, with uncertain status in MolluscaBase eds, 2026) and S. cf. malabonensis match lineage F with high similarity (99.8–100%); however, the correspondence between these nominal taxa and this lineage remains unresolved. Consequently, lineage F represents a well-supported molecular clade whose formal taxonomic identity still requires integrative revision, largely due to the high plasticity of shell morphology and the lack of reliable diagnostic characters.
It should be noted that once the identity of Saccostrea lineage F is clarified, the Colombian material will need to adopt the name corresponding to that lineage. Therefore, Colombian populations may represent an introduced Indo-Pacific lineage, most likely linked to maritime transport and fouling communities on ships, docks, and marinas. The coincidence of sequences from several locations is consistent with multiple introductions (probably independent in several ports/marinas) or with a secondary expansion from an initial focus in the Western Atlantic.
Several Saccostrea species have shown invasive potential worldwide, and records from Panama, Colombia, and Brazil indicate their ability to establish in new regions. The introduction of Saccostrea to Colombia poses potential ecological risks to native oyster species (C. rhizophorae, C. virginica, and others), which could face competition for space and resources. This case underscores the need to genetically characterize Colombian populations to determine their lineage, monitor the spread of these oysters in natural (mangroves, rocky shores) and artificial habitats (ports, marinas, pilings), and assess their ecological impacts on native oyster banks, benthic communities, and artisanal fisheries.
In the context of the presence of Saccostrea in MCL, the factors underlying its introduction and the timing of this event remain uncertain. This observation coincides with the recent appearance of other species, such as the sponge Amorphinopsis atlantica Carvalho, Hajdu, Mothes, and van Soest, 2004, which, although native to the Atlantic Ocean, had never been recorded in the area and is now conspicuous on mangrove roots (Paternina-Ramos et al., Reference Paternina-Ramos, Gracia, Pacheco-Medina, Gutiérrez and Zea2026). In Brazil, this sponge has been reported to exhibit invasive behaviour in Iguape Bay, where it thrives in estuarine environments with fluctuating salinity (Veloso-Junior et al., Reference Veloso-Junior, Pinto, Silva, Neves, Santana and Menegola2023). Likewise, the mussel M. strigata was detected during our surveys; it is now abundant in MCL (on roots and soft bottoms) and throughout the Colombian Caribbean, although no records of its presence existed prior to 2012 (Puyana et al., Reference Puyana, Prato and Díaz2012). In contrast, populations of Crassostrea have declined sharply. While previously never considered rare, this genus is now scarce and difficult to find, at least with the typical morphology once characteristic of Crassostrea species. This apparent decline of Crassostrea in occurrence and morphological consistency may reflect environmental degradation, increased competition with non-native oysters, or shifts in habitat availability across estuarine systems.
The changes in the MCL appear to have unfolded within the last 5–7 years. Local fishers (pers. comm. 2024–2025) report that neither Amorphinopsis nor Mytella was observed before this period, whereas Crassostrea was formerly abundant and widely harvested for consumption. This pattern suggests that a disturbance occurred in the lagoon, facilitating the establishment of new species while contributing to the ‘decline’ of Crassostrea, either through overexploitation or competitive displacement. Potential drivers include pollution, increased suspended matter, and salinization. However, the absence of continuous environmental monitoring prevents identification of the precise mechanisms. The only documented evidence is provided by MinAmbiente (2024) report, which indicates that in 2018 fishers and residents blocked the natural inflow of freshwater from Arroyo León stream into the estuary as a protective measure. This action could increase salinity and alter aquatic conditions. Additionally, the area surrounding MCL has experienced rapid urban expansion. Construction began in 2019, with a projected 16,000 housing units over an area of 80 hectares. Collectively, these alterations may have triggered a cascade of ecological changes that favoured species with invasive/opportunistic-like traits (e.g. the sponge and Mytella) or recognized invasive species (Saccostrea).
To date, five exotic marine and brackish mollusc species have been recorded in Colombia (Gracia et al., Reference Gracia, Medellín-Mora, Gil-Agudelo and Puentes2011, Reference Gracia, Pacheco-Medina, Paternina-Ramos, Peña-Granados and Rangel-Buitrago2024): the bivalves Electroma sp., Corbicula fluminea (O. F. Müller, 1774), Perna perna (Linnaeus, 1758), P. viridis (Linnaeus, 1758), and the gastropods Naria turdus (Lamarck, 1810) (Gracia et al., Reference Gracia, Pacheco-Medina, Paternina-Ramos, Peña-Granados and Rangel-Buitrago2024) and Eualetes tulipa (Rousseau, 1843) (Gracia and Paternina-Ramos, Reference Gracia and Paternina-Ramos2026). However, the Ministry of Environment and Sustainable Development, under Resolution 0067 of 2023, officially recognizes only the mussel Electroma sp. as an exotic invasive marine species in the country. This discrepancy highlights the need for continuous taxonomic, molecular, and ecological assessments to verify species identity, distribution, and invasion status. Further studies are required to clarify the current situation of each of these species, to conduct population analyses, and to better understand the ecological effects of their presence in different coastal systems.
A comprehensive synthesis of non-native molluscs in South America conducted by Darrigran et al. (Reference Darrigran, Agudo-Padrón, Baez, Belz, Cardoso, Carranza, Collado, Correoso, Cuezzo, Fabres, Gutiérrez-Gregoric, Letelier, Ludwig, Mansur, Pastorino, Penchaszadeh, Peralta, Rebolledo, Rumi, Santos, Thiengo, Vidigal and Damborenea2020) identified 86 introduced species, of which 14 occur in marine environments. More recently, the gastropod N. turdus has been recorded in the Caribbean (Dekkers and Ros, Reference Dekkers and Ros2022; Oleinik, Reference Oleinik2023; Oleinik et al., Reference Oleinik, Leal, DuPont and Uthairat2023), and Electroma vexillum (Reeve, 1857) was reported from Brazil (Rocha-Barreira et al., Reference Rocha-Barreira, Silva, Oliver, Carvalho, Menezes and Brito2025), further expanding the list of non-native molluscs documented in the region. Darrigran et al. (Reference Darrigran, Agudo-Padrón, Baez, Belz, Cardoso, Carranza, Collado, Correoso, Cuezzo, Fabres, Gutiérrez-Gregoric, Letelier, Ludwig, Mansur, Pastorino, Penchaszadeh, Peralta, Rebolledo, Rumi, Santos, Thiengo, Vidigal and Damborenea2020) listed invasive bivalve families, including Dreissenidae: Mytilopsis leucophaeata (Conrad, 1831); Isognomonidae: Isognomon bicolor (C.B. Adams, 1845); Mytilidae: Arcuatula senhousia (Benson in Cator, 1842) [=Musculista senhousia], Mytilus galloprovincialis Lamarck, 1819, Perna viridis (Linnaeus, 1758); Ostreidae: Crassostrea gigas (Thunberg, 1793), Talonostrea talonata X.-X. Li and Z.-Y. Qi, 1994, Saccostrea sp.; and Pectinidae: Pecten maximus (Linnaeus, 1758). Of these, only P. viridis has been recorded in the Caribbean (Darrigran et al., Reference Darrigran, Agudo-Padrón, Baez, Belz, Cardoso, Carranza, Collado, Correoso, Cuezzo, Fabres, Gutiérrez-Gregoric, Letelier, Ludwig, Mansur, Pastorino, Penchaszadeh, Peralta, Rebolledo, Rumi, Santos, Thiengo, Vidigal and Damborenea2020; Gracia and Rangel-Buitrago, Reference Gracia and Rangel-Buitrago2020). These findings highlight the likelihood of additional species being introduced to Colombian coasts through diverse vectors and underscore the urgent need to continue conducting baseline studies and medium- and long-term monitoring to enable early detection, since once established, eradication of invasive molluscs becomes extremely difficult, if not impossible.
Conclusions
The present study provides new advances in the knowledge of Ostreidae in the central Colombian Caribbean, confirming the presence of C. virginica and reporting for the first time the oyster Saccostrea lineage F in Colombia. Integrative taxonomy, combining morphological and molecular approaches, proved essential to clarify species identity and to distinguish C. virginica from its congener C. rhizophorae, which has at times been synonymized with the former species. Further research is needed to assess the current distribution of these species in MCL, other areas of the Atlántico Department, and throughout the Colombian Caribbean, as well as to clarify the identity of native oyster species, which is essential for the development of effective management strategies.
The Colombian finding aligns with other reports from Panama and Brazil, strengthening evidence of Saccostrea expansion into the tropical Western Atlantic. The detection of Saccostrea lineage F in both natural and artificial substrates highlights the role of maritime activities as potential introduction pathways and calls attention to the risks posed by non-native species to native oyster populations and coastal ecosystems.
The ecological transformations observed in MCL over the past decade highlight a dynamic shift in community structure, marked by the possible decline of native Crassostrea populations and the concurrent emergence of species such as Saccostrea lineage F, M. strigata, and A. atlantica. These changes, occurring within a relatively short time frame, suggest the influence of recent anthropogenic disturbances. While the absence of continuous environmental monitoring prevents a precise identification of drivers, the evidence points to a cascade of ecological effects that have favoured opportunistic or invasive species. This case underscores the urgent need for long-term ecological monitoring and integrated management strategies to safeguard the resilience of coastal lagoons under mounting anthropogenic and climatic pressures.
The Colombian record adds to the growing list of non-native molluscs in northern South America and emphasizes the urgent need for integrative taxonomy and monitoring programmes to detect, track, and mitigate the impacts of invasive marine species.
Supplementary material
The supplementary material for this article can be found at https://doi.org/10.1017/S0025315426101519.
Acknowledgements
We thank the Museo de Historia Natural Marina de Colombia – Makuriwa, INVEMAR, for accessioning the material, with special thanks to E. Montoya and M. Martelo for their support. We express our gratitude to the fishermen of the Mallorquín Coastal Lagoon for their assistance during fieldwork and for sharing their valuable knowledge. This work is a contribution from the research group ‘Geología, Geofísica y Procesos Marino-Costeros’, Universidad del Atlántico.
Author contributions
A.G.C.: Conceptualization, methodology, data curation, formal analysis, investigation, writing – original draft preparation, writing – review and editing, funding acquisition; A.P.R.: Conceptualization, methodology, data curation, formal analysis, investigation, writing – original draft preparation, writing – review and editing; K.P.M.: Conceptualization, methodology, data curation, formal analysis, investigation, writing – original draft preparation, writing – review and editing; G.R.N.S.: Formal analysis, writing – review and editing; N.S.: Formal analysis, writing – review and editing; J.D.F.: Methodology, formal analysis, writing – review and editing.
Declaration of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Data availability statement
All data supporting the findings of this study are available within the paper and its supplementary information.
Ethics and approach
The material was collected under the biological specimen collection permit granted to the Universidad del Atlántico by ANLA, based on Resolution 1214 of September 29, 2017, and Resolution 00594 of April 26, 2018.
Funding statement
This work was partially supported by Universidad del Atlántico (A.G.C., grant number CB410-CII2022). Additional support was provided through the project ‘Organismos marinos con potencial invasor en el Caribe colombiano (Fase 1)’, funded under the Universidad del Atlántico’s internal call ‘Convocatoria interna para el fortalecimiento de grupos de investigación con herramientas para la creación, la innovación y la investigación – 2021’. The remaining portion of the work was funded by the lead author through the self-funded project ‘El litoral del Departamento del Atlántico (Colombia): LDA’.
