Abstract
Biological invasions are globally recognized as one of the main drivers of biodiversity loss. Over the past four decades, there has been significant progress in understanding the mechanisms of alien species introduction into marine and estuarine environments. It is currently known that although humans can spread non-native species in various ways (e.g. aquaculture, vessel biofouling and oil and gas activities), ballast water is one of the most effective being considered one of the main threats to marine biodiversity. This pathway also appears to be the main transport vector to explain the spread of the exotic bivalve Theora lubrica (or Asian Semele) since the late 1950s. In this study, we report for the first time the presence of Asian Semele in the Southwestern Atlantic, specifically along the Southeast coast of Brazil. Furthermore, we also provide new insights into shell morphology, gross anatomy and ecological aspects, as well as the updated global distribution of this invasive alien species.
1 Introduction
Hundreds of exotic species are likely introduced annually worldwide, with ports as the primary entry point and ballast water being one of the most effective means of transport (; ). Some ports host more non-native species than native ones, with certain introduced species displaying massive colonization, gradually contributing to global biotic homogenization ().
In South American countries, unlike those in the NE Atlantic, there is a lack of ongoing projects or comprehensive studies on alien marine species. Even so, new records of exotic marine species in Brazil, Argentina, and Uruguay have increased over the past two decades (; ). For Brazil, specifically, 63 non-native marine and/or estuarine species are recorded, of which 15 are categorized as invasive, 11 of which are bivalves species (>70%), the oysters Isognomon bicolor (C. B. Adams, 1845), Magallana gigas (Thunberg, 1793), Saccostrea cuccullata (Born, 1778), Crassostrea virginica (Gmelin, 1791), and the mussels Xenostrobus securis (Lamarck, 1819), Leiosolenus aristatus (Dillwyn, 1817), Mytilus galloprovincialis Lamarck, 1819, Mytilopsis cf. sallei (probably a species complex), Mytilopsis leucophaeata (Conrad, 1831), Perna perna (Linnaeus, 1758) and Perna viridis (Linnaeus, 1758) (; ; ; ; ; ; , ).
In general, bivalves are regarded as efficient invaders and ecosystem engineers, sometimes capable of drastically altering the environment (; ). This invasive potential has already been well documented in Brazilian waters, especially for larger and epifaunal species (). However, studies on exotic species—whether invasive or not—that are small (<1 cm in length) and infaunal are rare. In this context, the present work provides the first record of the tiny bivalve Theora lubrica A. commonly known as the Asian Semele, in the Southwestern Atlantic. Morphological descriptions, ecological notes, and updates on the global distribution of this invasive species were also addressed here.
2 Materials and methods
2.1 Sampling site
Ranked among the 20 ports with the highest risk of biological invasions, the Port of Santos is located within the Santos Estuary, between the municipalities of Santos, Cubatão, and Guarujá in Southeastern Brazil (). The port features several terminals for cargo storage and handling, boasting the largest container traffic in Brazil and connections to over 600 ports worldwide (). As expected for estuarine areas with high human impact, the water column surrounding the port exhibits low dissolved oxygen levels, elevated concentrations of nitrogen, phosphorus, and organic matter, along with harmful chemical elements, with areas of the estuary ranging from mesotrophic to eutrophic (; ). As is typical in port areas, the Port of Santos and its surrounding regions also report annual increases in the number of exotic aquatic species (). Since 2017, however, the Port has implemented and consistently maintained an on-site bioinvasion monitoring project to track and mitigate alien species ().
2.2 Sorting and morphological analysis
All 10 individuals of Theora lubrica with preserved internal tissues were provided by a consultancy project (Econsult Estudos Ambientais) aimed to evaluate the benthic fauna of the estuarine areas surrounding the Port of Santos. The specimens were collected from only three of the 50 stations covered by the port monitoring project, between December 2023 and May 2024. Samplings were performed in soft substrata at depths ranging from 4.5 to 15.6 meters, using a Petersen grab (0.058 m²), with three replicates in each of the three stations. Water parameters such as temperature, salinity, pH, conductivity, dissolved oxygen and turbidity, were measured in each station. The samples were sieved in the field and stored in 70% ethanol. The shells and soft parts of T. lubrica were photographed using a motorized Nikon SMZ25 stereomicroscope equipped with a Nikon Digital Sight 10 camera; images were stacked using Nikon NIS Elements Basic Research (v. 5.42.04) software. Some well-preserved valves were also selected for hinge characterization using a Hitachi TM4000 Plus tabletop SEM. The material is archived at Museu de Zoologia da Universidade Estadual do Norte do Paraná, under the numbers UENP 2935–2936.
2.3 Taxonomy comparisons and examined specimens
Being an exotic species widely distributed around the globe, the specimens collected in Brazil were compared with all morphologically similar species of the genus Theora, as well as with Abra nitida (O. F. Müller, 1776). The latter, although never recorded in the Southwestern Atlantic, has an outline resembling that of T. lubrica. Type series of the most similar species, including Theora lata (Hinds, 1843) (Holotype - USNM 535) and Abra prismatica (Syntype - EXEMS Moll3731-5), were also examined. A redescription of the shell of T. lubrica, including the hinge teeth details, was provided due to the lack of high-resolution images in the literature; tooth numbering followed . General anatomical features, including details of the internal tissues, were provided for the first time. It is important to note that, due to their small size and extremely fragile shells, individuals of T. lubrica can easily be broken during sampling and/or misidentified as juveniles of other species of the Tellinoidea. The authors FMM and CMS also identified specimens of T. lubrica from Northeastern Brazil (state of Bahia); however, precise collection data are not currently available for publication.
3 Results
The specimens of Theora lubrica were sampled in three stations (sta. P11: Santos Port channel; sta. P20 and PD10: Largo do Canéu - inner part of the Santos Estuary) at the Port of Santos - Southeastern Brazil. All information regarding the stations and water parameters is compiled in Table 1, which indicates that these specimens inhabit a polyhaline environment (18-30 ppt) in a subtidal zone, tolerating a wide range of dissolved oxygen concentrations (3-15 mg/L).
Table 1
| Parameters | Stations | ||
|---|---|---|---|
| P11 (23.9335°S, 46.30833°W) | P20 (23.9127°S, 46.36433°W) | PD10 (23.91453°S, 46.3648°W) | |
| Date/time | 12/Jun/23 | 12/Jun/23 | 22/May/24 |
| 13:20 | 12:13 | 13:05 | |
| Tides | Ebb tide | Ebb tide | Flood tide |
| Depth (m) | 4.5 | 14.5 | 15.6 |
| Air temperature (°C) | 35.7 | 35.4 | 30.3 |
| Water temperature (°C) | 27.8 | 28.8 | 26 |
| pH control | 7.4 | 7.6 | 7.2 |
| Conductivity (µS/cm) | 37.700 | 29.500 | 44.200 |
| Turbidity (NTU) | 2 | 5.7 | 2.6 |
| Oxygen dissolved (mg/L) | 10.98* | 14.4* | 2.92 |
| Salinity (ppt) | 24.2 | 18 | 28.5 |
Set of measurements of water parameters at the three sampling stations in the Port of Santos – Brazil.
*High oxygen concentrations attributed to microalgae bloom.
3.1 Taxonomy
Superfamily Tellinoidea Blainville, 1814
Family Semelidae Stoliczka, 1870
Genus Theora H. Adams & A. Adams, 1856
Figure 1
Figure 2
Diagnosis of Theora
Shell thin, hyaline, smooth, gaping on at least one side. Anterior end rounded; posterior end produced. Hinge with one to three cardinal teeth; lateral present in at least one valve. Chondrophore projecting. Deep pallial sinus confluent with pallial line (after ; ).
3.2 Shell redescription
Shell small up to 16 mm (Brazilian specimens, 2.8 to 10.3 mm in length), thin, elongated, semi-transparent and elliptical. Equivalve, inequilateral, umbones slightly anterior, pointed and prominent; larval shell, reniform, whitish, smooth and well-preserved (290 ± 30µm n=6), prodissoconch I (80 ± 10µm n=6) and II boundary only visible in SEM (Figures 1A, B, E, 2A–C). Outer surface smooth, whitish with a shiny periostracum; shell bears fine, concentric lines; internal anterior ridge visible (r), mainly in dry shells (Figures 1A, B, 2A, B). Valves gape slightly at the anterior and posterior ends (ag, pg); lunule and escutcheon absent (Figure 2C). Inner surface whitish and shiny with a thickened internal ridge (r) extending obliquely across the shell, anterior to the umbo. Right valve with two divergent cardinal teeth (3a, 3b) and a single anterior and posterior lateral (AI, PI) (Figures 1C, E). Left valve with three cardinal teeth: a smaller posterior-dorsal one (4b), a middle-ventral, robust, trigonal (2b), and an anterior elongated and laminate (2a), sometimes covered by periostracum (pe); including a single anterior and posterior lateral (AII, PII) (Figures 1D, F). Hinge plate narrow with a projecting spoon-shaped chondrophore (c), to which is attached a robust internal ligament (il) (Figures 1E, F). External ligament (el) brownish and short (Figures 1B, 2C). Pallial sinus deep, extends beyond the mid dorso-ventral axis of the shell, confluent with pallial line.
3.3 Gross anatomy
Mantle lobes with three marginal folds (inner, middle and outer) completely unattached antero-ventrally, forming an extensive pedal opening. The middle sensorial fold bears a single row of numerous short, digitiform mantle tentacles (mt) distributed along the mantle margins, except on the dorsal margin (Figure 2). Posteriorly, two long, cylindrical and completely separated siphons probably formed by the fusion and hypertrophy of the inner folds of the mantle, i.e. Type A (, ). Siphonal retractor muscles (srm) present. Inhalant siphon (is) thicker, ventral and larger than the exhalant siphon (es). Cruciform muscle (cm) near the base of the inhalant siphon forming the only fusion of the ventral mantle margin. A pair of symmetric and bilateral siphonal organs (so) located close to the proximal aperture of the inhalant siphon on both sides. Ctenidia (ct) eulamellibranch, complete with outer and inner demibranchs (id/od). Labial palps (lp) trigonal, large, similar in size with gills; outer and inner palps present. Adductor muscles unequal; the anterior (aam) thin and elongated dorsoventrally and the posterior (pam) oval. Foot (f) wide, with a ventral surface (sole), posterior pedal retractor muscle (pprm) attached to the shell close to the posterior adductor muscle, insertion of the anterior pedal retractor muscle not visible; byssal thread absent. A few aspects of the visceral mass were also observed such as digestive diverticula (dd), hind gut (hg), kidney (k) and probably ovary (ov)? and testis (te)? seen only by transparency (Figures 2D, E).
4 Discussion
4.1 Morphological remarks
The shell features of Theora lubrica have been extensively documented in the literature, including its shape, coloration, external and internal sculpture, as well as its ligament and hinge teeth (; ; ; ; ). However, it seems that for over 130 years, the hinge teeth of this species have been misinterpreted, probably due to the absence of descriptions using SEM. In virtually all recent descriptions (; ), the right valve is reported to have two cardinal teeth, while the left valve is described as having only one cardinal tooth. Our description, therefore, demonstrates for the first time that the left valve actually has three cardinal teeth (2a, 2b, 4b) (Figures 1D, F). Furthermore, it hypothesizes the numbering/labeling of all hinge teeth based on their position and appearance during ontogeny, following . It is also important to note that the tooth characterized here as ‘4b’ has been previously observed and illustrated by : Figure 4 but was probably interpreted as a secondary tooth. The tooth ‘2a’, observed here for the first time, may eventually become covered by periostracum (pe) in some individuals, which could make it difficult to visualize (Figure 1D). This partly explains its absence in previous descriptions. Our literature review also indicated that T. lubrica specimens collected worldwide from 1861 to the present have a shell ranging from 2 to 16 mm in length. However, shells measuring up to 20 mm were also reported in the literature by , p. 438), but we were unable to access these specimens.
Limited information on the anatomy of T. lubrica is available in the literature, including features on the siphons (coloration and length) of specimens from the UK (), a few photos showing the soft parts through the shell’s transparency (: Figure 2A; : Figure 3; : Figures 2, 3), and histological sections of gonads of individuals from New Zealand (: plates 3.1-3.3 – master thesis). Here, for the first time, detailed information on the pallial cavity organs and visceral mass is provided, bringing potential new insights into the functional morphology of T. lubrica (Figures 2D, E). Among the main anatomical characteristics of T. lubrica, the following stand out: (i) the presence of numerous small tentacles along the mantle margins, (ii) a bilateral siphonal organ, and (iii) indirect evidence of hermaphroditism.
Figure 3
Generally, bivalves exhibit a great diversity of tentacles along their mantle margins, typically associated with sensory or secretory functions (; ). Similar to T. lubrica, other members of the superfamily Tellinoidea also have small tentacles (or papillae) along the free mantle edges such as Austromacoma biota (Arruda & Domaneschi, 2005), Tellina angrensis (), Temnoconcha brasiliana (Dall, 1921) (; ; ) and the confamilial species Abra alba (W. Wood, 1802), Scrobicularia plana (da Costa, 1778), Semele purpuracens (Gmelin, 1791), Semele proficua (Pulteney, 1799) and Semele trindadis Simone, 2021 (; ; ). For both species, the function of these mantle tentacles is uncertain, but two hypotheses may be considered: (i) acting as sensory tentacles regulating the opening and closing of the shell during digging process or (ii) producing mucus to aid in the removal of excess and rejected particles from the pallial cavity.
For the first time a pair of siphonal organs was observed in a member of the family Semelidae. Theora lubrica is, therefore, the first semelid known to possess a bilateral siphonal organ, a condition previously observed only in Macoma biota (Tellinidae) (). The presence of a single asymmetric siphonal organ appears to be a more common condition among Tellinoidea, having received different names since its first description by . The terms ‘valvulae palleale’, ‘siphonal membrane’, ‘mantle folds’, ‘parasiphonal organ’ and ‘pseudogills’ have also been used to refer to a possibly homologous structure among members of this superfamily (; ; ; ; ). The function of the siphonal organs was first elucidated by in Rexithaerus secta (Conrad, 1837), demonstrating that it assists in the removal of waste matter. Almost 100 years later in M. biota, also attributes the same function to these organs, “the siphonal organs increase the superficial area of the mantle, agglutinate a large quantity of particles eliminated by the pallial organs and convey this material to the waste channel”. This is a crucial function in deposit-feeders like Theora lubrica, where large amounts of sediment and pseudofeces often accumulate in the pallial cavity.
Theora lubrica was characterized as a dioecious species by and ; however, the individuals sampled in Brazil apparently exhibit both types of gonads (ovaries and testes) simultaneously (Figure 2D). It is important to note that this potential hermaphroditic condition is based solely on an analysis of gross anatomy and still needs future confirmation.
4.2 Biology and ecological notes
Although live specimens of T. lubrica were not analyzed in this study, a brief review of key aspects of its ecology is provided. Essential information on the species’ population dynamics and biology is compiled, which may support the future development and implementation of methods for the control and/or eradication of this invasive alien species in the Global South.
Theora lubrica (or Asian Semele) is a small, infaunal bivalve that typically occurs in soft, muddy subtidal or lower intertidal sediments rich in organic matter. It is buried at depths of 10 to 30 mm in the substrate and feeds on benthic algae and detritus (). The maximum burrowing depth suggests that in living specimens the relatively long and thin siphons of T. lubrica can extend two to three times the length of the shell. This species tolerates high variations in salinity and can therefore be classified as a marine (30-40 ppt) or estuarine (18-30 ppt) (; ; ; ; the present study). Their populations often exhibit significant fluctuations in density, ranging from 30-70 individuals/m² to as many as 2,000/m² (; ). Such fluctuations, observed in New Zealand and Japan, appear to be strongly linked to water and sediment temperature, as well as low oxygen levels, with faster growth rates in summer compared to winter and significant diebacks during the warmer months. Considerable population declines have also been linked to high predation rates by a mud crab in New Zealand ().
T. lubrica is a fast-growing dioecious species; its individuals can mature in 1 to 3 months, at about 4-7 mm (; ). The larval prodissoconch size (PI = 80 ± 10µm) of individuals collected in Brazil indicates that T. lubrica probably has an indirect and planktotrophic development (see ). Although there is no record of studies on the development of T. lubrica, showed that the congener Theora lata (Hinds, 1843) has planktotrophic larvae that spend about 13 days in the plankton at 24°C. The Asian Semele is also a short-lived species that can rapidly colonize disturbed and muddy habitats and is among the most pollution-tolerant mollusks found in some harbors in New Zealand, thriving even in contaminated sediments (). Due to its frequent dominance in highly polluted environments, T. lubrica is regarded as a pollution-indicator species.
Although T. lubrica has been reported as one of the two worst invasive mollusks in Europe by , no ecological or economic impacts have yet been documented for this species. Even so, it is worth noting that species with the invasive potential of T. lubrica can cause aggressive colonization in short periods of time, gradually leading to global biotic homogenization of the environment (). According to , ‘billions’ of individuals were observed living in Waitemata Harbour – New Zealand, where T. lubrica is one of the few species capable of tolerating the polluted sediments.
4.3 Global distribution
Theora lubrica is native to the Northwest Pacific (NWP), ranging from northern Japan (Hakodate Bay, type locality) and the Vladivostok area in Russia, to the Hong Kong region (; ; ) but over the last 60 years it has been constantly introduced into various parts of the world (; ; ; ; ; ; ; ). Figure 3 provides an up-to-date overview of the distribution of this species, including all known localities around the globe. Currently T. lubrica is spread mainly in port regions of Australia (AUS), New Zealand (NZ), Northeast Pacific (NEP), Mediterranean (MED), Northeast Atlantic (NEA) and now in the Southwestern Atlantic (SWA). Although the new record was made for Southeast Brazil, it is worth noting that individuals of T. lubrica from Northeast Brazil were also identified by FMM and CMS, first and second author respectively. In both cases, ballast water is probably the main factor responsible for the introduction of this exotic species into Brazilian waters.
Like many other invasive species, although it does not exhibit phenotypic plasticity, T. lubrica displays other typical traits of r-strategists, such as small body size, early sexual maturity, rapid gametogenesis, an almost continuous breeding season with multiple cohorts, planktotrophic larvae that can potentially remain in the water column for up to 20 days, opportunistic and gregarious behavior, and a wide tolerance to environmental stress (; ).
Despite being well established in the literature, the concept of invasive species () can be difficult to apply, often due to taxonomic issues or the lack of ecological studies for some species. However, given its small shell size, which hinders identification, and its invasive potential, there is no doubt that T. lubrica should be considered an invasive species that may have already spread across much of Brazil and other countries in South America. In this way, both alien species monitoring, and ballast water treatment should be carried out continuously to prevent the spread of T. lubrica throughout the Global South, including the warmer waters of the Caribbean. Currently, among the main port countries in South America, only Brazil and Argentina are signatories to the Ballast Water Management Convention (BWMC) – a treaty adopted to help prevent the spread of potentially harmful aquatic organisms and pathogens in ships’ ballast water (). Therefore, broad adherence to this treaty is essential for preserving South America’s native aquatic fauna and avoiding the potential introduction of other invasive aquatic species.
Finally, this new record of T. lubrica expands the list of invasive species in the Southwest Atlantic and helps fill part of the huge knowledge gap on alien species in the Global South.
Statements
Data availability statement
The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.
Ethics statement
Ethical approval was not required for the study involving animals in accordance with the local legislation and institutional requirements because studies involving small, exotic, and abundant marine invertebrates in Brazil do not require ethical approval.
Author contributions
FM: Conceptualization, Data curation, Methodology, Supervision, Writing – original draft, Writing – review & editing. CS: Writing – review & editing, Data curation. FO: Writing – review & editing, Data curation. MM: Writing – review & editing. TV: Writing – review & editing. VC: Funding acquisition, Project administration, Writing – review & editing. AL: Writing – review & editing, Funding acquisition, Project administration. CY: Writing – review & editing. RS: Writing – review & editing. LN-J: Writing – review & editing, Funding acquisition, Project administration. LO: Writing – review & editing, Funding acquisition, Project administration.
Funding
The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This study received funding from Port of Santos, Tetra Tech and Econsult Estudos Ambientais.
Acknowledgments
The authors are grateful to the Senckenberg Ocean Species Alliance (SOSA) for providing access to electron and optical microscopy facilities, as well as to Jan Steger for his technical advice. Special thanks are also extended to Michela Borges (MDBio/UNICAMP) for granting access to microscopy facilities during the initial stage of the project. Special thanks are due to Tetra Tech América do Sul and Porto de Santos for providing access to the samples. Thanks are due to IBAMA (Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis) for supporting the ongoing monitoring of exotic species along the Brazilian coast. We also thank the entire team at the benthic invertebrate screening laboratory and the technical team at Econsult Estudos Ambientais.
Conflict of interest
Authors CS, FO, MM, TV, and VC were employed by company Econsult Estudos Ambientais. Authors AL, CY, and RS were employed by company Tetra Tech. Authors LN-J and LO were employed by company Port of Santos.
The remaining author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
The authors declare that this study received funding from Tetra Tech, Econsult Estudos Ambientais and Port of Santos. The funders had the following involvement in the study: collection, analysis and interpretation of data and decision to submit it for publication.
Generative AI statement
The author(s) declare that no Generative AI was used in the creation of this manuscript.
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Summary
Keywords
non-native bivalves, Asian Semele, Mollusca, shell morphology, gross anatomy, polyhaline mollusks, biomonitoring and environmental monitoring
Citation
Machado FM, Suga CM, Onodera FKC, Melo MS, Viti T, Cavinatto VM, Lammardo ACR, Yonamine CY, Sáfadi RS, Nogueira-Junior LA and Oliva LFM (2025) Spreading further: the first record of the alien bivalve Theora lubrica in the Southwestern Atlantic Ocean. Front. Mar. Sci. 12:1511313. doi: 10.3389/fmars.2025.1511313
Received
14 October 2024
Accepted
31 January 2025
Published
27 February 2025
Volume
12 - 2025
Edited by
Katherine Dafforn, Macquarie University, Australia
Reviewed by
Francesco Tiralongo, University of Catania, Italy
Daniel Cavallari, University of São Paulo, Brazil
Updates
Copyright
© 2025 Machado, Suga, Onodera, Melo, Viti, Cavinatto, Lammardo, Yonamine, Sáfadi, Nogueira-Junior and Oliva.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Fabrizio Marcondes Machado, fabriziomarcondes@yahoo.com.br
†ORCID: Fabrizio Marcondes Machado, orcid.org/0000-0002-5085-865X; Cristiane Midori Suga, orcid.org/0009-0009-8598-3504; Fabio Kiyoshi Camara Onodera, orcid.org/0009-0002-7834-1027; Mariana Sousa Melo, orcid.org/0000-0002-5546-2718; Thais Viti, orcid.org/0009-0008-9362-9030; Vilma Maria Cavinatto, orcid.org/0009-0009-1982-7407; Ana Carolina da Rocha Lammardo, orcid.org/0009-0004-8963-0638; Carolina Yumi Yonamine, orcid.org/0009-0002-5826-6963; Regina Sawaia Sáfadi, orcid.org/0009-0001-6482-9796; Luis Antonio Nogueira-Junior, orcid.org/0009-0002-1876-1820; Luiz Fernando Maciel Oliva, orcid.org/0009-0003-2857-6239
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