Records of the invasive sun coral Tubastraea and migration offshore-onshore in an estuarine zone of northeastern Brazil

Registros do coral sol invasor Tubastraea e migração offshore-onshore em uma zona estuarina do nordeste do Brasil

Abstract:

Invasive corals of the genus Tubastraea exhibit early maturity, rapid growth, and plasticity regarding the substrate they use, which has enabled the genus to quickly become successful and expand its non-native range. For the state of Sergipe there are 23 records of Tubastraea spp. on oil platforms; here we report the first records of the sun coral T. coccinea on the coast in the estuarine zone of the Vaza-Barris River, expanding its invasive range from offshore to onshore. Contaminated oil platforms, vessels, and shipwrecks may have provided a pathway as vectors, acting as stepping stones that connect oceanic regions to the coast. Dispersal may also occur through currents responsible for transporting organisms from the continental shelf to the coast, although this seems unlikely. Thus, we reinforce the importance of constant monitoring of vectors and the coast to minimize the adverse effects of invasive corals on native fauna.

Keywords: Non-native; Coral reef; Invasion; Dispersion; Range expansion; Oil platform

Resumo:

Corais invasores do gênero Tubastraea apresentam maturidade precoce, rápido crescimento e plasticidade em relação ao substrato que utilizam, o que permitiu ao gênero obter rapidamente sucesso e expandir sua distribuição não nativa. Para o estado de Sergipe existem 23 registros de Tubastraea spp. na zona offshore; aqui relatamos os primeiros registros do coral-sol T. coccinea na costa da zona estuarina do rio Vaza-Barris, expandindo sua área de invasão offshore para o onshore. Plataformas petrolíferas, navios e naufrágios contaminados podem ter fornecido o caminho como vetores, agindo como trampolins que ligam as regiões oceânicas à costa. A dispersão também pode ocorrer através de correntes responsáveis pelo transporte de organismos da plataforma continental para a costa, embora isto pareça menos provável. Assim, reforçamos a importância do monitoramento constante dos vetores e da costa para minimizar os efeitos adversos dos corais invasores sobre a fauna nativa.

Palabras clave: Não-nativos; Recifes de coral; Invasão; Dispersão; Expansão de Distribuição; Plataforma petrolífera

Introduction

The global vessel transport network has led to the introduction of non-native species, mainly through biofouling and ballast water (Ferrario et al. 2017). The advancement of international maritime trade (i.e. 80% of all goods traded worldwide) has resulted in an increase in routes that enable non-native species to cross geographical barriers and their subsequent establishment (Hulme 2021). A notable number of successful marine invasions have occurred in coastal regions worldwide (Santos et al. 2023), including Sargassum horneri (Marks et al. 2020), Limnoperna fortunei (Wang et al. 2024), Branchiomma luctuosum (Mabrouki et al. 2021), Mnemiopsis leidyi (Shiganova et al. 2019), and Diplosoma listerianum (Lowen & DiBacco 2023). The establishment of these species in environments outside their natural range has caused changes in the composition and abundance of the receiving communities (Lages et al. 2011) and has substantially affected the economy, with an annual cost of approximately 146.5 billion dollars worldwide (Diagne et al. 2021).

Azooxanthellate corals of the genus Tubastraea (Scleractinia: Dendrophylliidae) are native to the Indo-Pacific region. Currently, some of its species are invasive in the coastal areas of the Gulf of Mexico, the Caribbean Sea, and the Northeast and Southwest Atlantic (Costa et al. 2014, López et al. 2019, Bastos et al. 2022). The introduction of Tubastraea in the Atlantic is directly related to port activities and oil exploration, mainly through fouling of ships’ hulls and oil platforms and infrastructure that enabled the breaking of geographical barriers (Hewitt et al. 2009). Such invasive corals have successfully expanded their distribution locally because of their superior competitive strategies, early maturity, rapid growth, and plasticity in the use of different substrates (De Paula et al. 2014).

In Brazil, the first observations of species of the genus Tubastraea were made in 1980 on oil and gas platforms in the Campos Basin, state of Rio de Janeiro (southeastern Brazil) (Castro & Pires 2001). Later, other populations were discovered on rocky shores in Ilha Grande Bay and Arraial do Cabo, expanding our knowledge about the invasion of Tubastraea on the coast of southeastern Brazil (Meurer et al. 2010, Silva et al. 2014).

In northeastern Brazil, the invasive sun coral was first reported on the coast of the state of Bahia (Sampaio et al. 2012), where T. coccinea Lesson, 1830 and T. tagusensis Wells, 1982 co-occurred in Baía de Todos os Santos and within an estuarine complex (Miranda et al. 2016). These corals have also been reported on natural and artificial structures such as platforms and shipwrecks along the coast of the states of Ceará, Rio Grande do Norte, Pernambuco, and Alagoas (Soares et al. 2018, Miranda et al. 2020, 2022). Records of Tubastraea in the state of Sergipe have been limited to offshore oil platforms (Petrobras 2016, Creed et al. 2017, Coelho et al. 2022). The aim of this study was to provide a report of the migration offshore-onshore of T. coccinea and evaluate the directional range expansion of the Tubastraea invasion on the coast of Sergipe, northeastern Brazil.

Materials and Methods

^1.

Study area

The continental shelf of the state of Sergipe (11°5’59.17”S, 37°8’59.30”W) is about 170 km long, 12-35 km wide, has a gentle slope and an average depth of 41 m (Lemos Júnior et al. 2014, Soares et al. 2021). It is located between the São Francisco (to the north) and Piauí/Real (south) rivers (Lemos Júnior et al. 2014, Soares et al. 2021). This stretch is characterized as a depositional environment due to the presence of an extensive strip of sand separated by broad estuarine complexes (Soares et al. 2021), as well as for accommodating large sedimentary deposits (Lemos Junior et al. 2014). The shelf is mainly influenced by inputs from the estuaries of the São Francisco, Japaratuba, Sergipe, Vaza-Barris, and Piauí-Fundo-Real River complexes (Lemos Júnior et al. 2014, Santos et al. 2020), so most of the region has soft bottoms.

The Vaza-Barris River corresponds to a coastal drainage that reaches the Atlantic Ocean in the central region of the coast of the state of Sergipe (Santos & Latrubesse 2022) with an average annual flow of 7.51 m³/s (Oliveira & Souza 2015). The lower estuary (~5 km wide) is undergoing coastal urbanization driven by changes in coastal infrastructure, shipping, tourism, and recreation, which have resulted in an increase in artificial structures and vessel movement.

^2.

Data collection

To map the introduction of Tubastraea, we gathered information from technical reports on the monitoring of oil platforms on the coast of Sergipe (Petrobras 2016). Data spatialization was performed using the free software QGIS (QGIS Development Team 2023). Species, substrate, and date were also recorded.

Areas with artificial structures (e.g., wood, concrete, iron, plastic, and styrofoam) in the lower estuary of the Vaza-Barris River were inspected by snorkelling during high tide (neap tide, amplitude 1.7 m), totaling 22 sampled sites of diving (Figure 1). After the detection of the first colony, bimonthly monitoring was carried out at the site of detection and at other possible fouling sites marked on the map (Figure 1). These colonies were collected (SISBIO 24097-6) using a knife, stored in a plastic bag with water, and taken to the laboratory where they were preserved in 96% ethanol. Colonies and polyps were measured in the laboratory using a digital caliper according to Cairns (1991). Identification was performed based on De Paula & Creed (2004). The studied colonies were deposited in the Coleção Zoológica do Departamento de Biologia, Centro de Ciências Biológicas e da Saúde, Universidade Federal de Sergipe (CZUFS CN1-00393, CZUFS CN1-00523).

Figure 1.
Tubastraea in the Vaza-Barris River estuary: A. Map of the study area showing the Vaza-Barris River estuary and adjacent continental shelf with offshore records. B. Study area showing a stretch of the Vaza-Barris River estuary with sampled points (red points) and the new record (star). C. Photos showing the mouth of the Vaza-Barris River and the artificial structure (pier) on which the Tubastraea colony was recorded.

Results

The survey of data contained in technical reports resulted in 23 records of Tubastraea on oil platforms, as well as two records from our field collection in the estuarine area of the Vaza-Barris River (Figure 1, Table 1). These onshore records correspond to two colonies of T. coccinea fixed on an artificial substrate and photographed in situ on January 31 2023 and February 17 2024.

Table 1.
Records of the genus Tubastraea in offshore and inshore zones in the state of Sergipe, Brazil.

Site	Latitude	Longitude	Substrate	Number of colonies			Date	Source
				T. coccinea	T. tagusensis	Tubastraea sp.
PCB-1	−11.0082	−36.93273	Metal	16	2	0	2016	Petrobras (2016)
PCB-2	−11.00052	−36.92472	Metal	52	45	11	2016	Petrobras (2016)
PCB-3	−10.99598	−36.92368	Metal	3	4	0	2016	Petrobras (2016)
PCB-4	−11.00718	−36.92582	Metal	365	10	53	2016	Petrobras (2016)
PCM-2	−10.98452	−36.9822	Metal	97	0	37	2016	Petrobras (2016)
PCM-4	−10.9855	−36.96477	Metal	1	0	0	2016	Petrobras (2016)
PCM-5	−10.99952	−36.97212	Metal	11	2	0	2016	Petrobras (2016)
PCM-6	−10.9833	−3693287	Metal	133	85	0	2016	Petrobras (2016)
PCM-7	−11.01398	−36.98843	Metal	3	2	0	2016	Petrobras (2016)
PCM-8	−10.98808	−36.938	Metal	381	107	9	2016	Petrobras (2016)
PCM-9	−10.9871	−36.94847	Metal	77	0	24	2016	Petrobras (2016)
PCM-10	−10.97747	−36.95355	Metal	3	4	0	2016	Petrobras (2016)
PCM-11	−10.592473	−36.572121	Metal	69	55	1	2016	Petrobras (2016)
PGA-1	−11.14925	−37.04915	Metal	13	2	0	2016	Petrobras (2016)
PGA-2	−11.1645	−37.05257	Metal	97	101	5	2016	Petrobras (2016)
PGA-3	−11.14275	−37.03998	Metal	52	78	1	2016	Petrobras (2016)
PGA-4	−11.13175	−37.04753	Metal	0	2	3	2016	Petrobras (2016)
PGA-5	−11.15367	−37.06187	Metal	80	1	33	2016	Petrobras (2016)
PGA-7	−11.20232	−37.07955	Metal	168	91	693	2016	Petrobras (2016)
PGA-8	−11.17753	−37.0185	Metal	232	152	21	2016	Petrobras (2016)
PDO-1	−11.09837	−36.95975	Metal	2	3	0	2016	Petrobras (2016)
PDO-2	−11.11517	−36.96655	Metal	17	1	0	2016	Petrobras (2016)
PDO-3	−11.1199	−36.97897	Metal	253	85	0	2016	Petrobras (2016)
Vaza-Barris	−11.099789	−37.149829	Concrete	1	0	0	2023	Present study
Vaza-Barris	−11.099789	−37.149829	Concrete	1	0	0	2024	Present study

Colonies of T. coccinea were found repeatedly in the subtidal zone (about 2 m deep) in one site of the estuarine complex of the Vaza-Barris River (Figure 2, Supplementary Material https://figshare.com/s/8f5ab24af0145b4f7db3 (temperature 27.11 ± 2.93 ^oC and salinity 34.36 ± 3.57). These colonies were approximately 6 km from the mouth of the estuary and 25 km from the nearest offshore oil platforms (previously known occurrences) strongly fixed to a vertical artificial concrete structure (pier) at Orla Por do Sol, Aracaju, state of Sergipe.

Figure 2.
Specimen of Tubastraea coccinea sampled in the estuary of the Vaza-Barris River. (A) Image recorded in the laboratory. (B) Fixed colony listed in the zoologic collection (CZUFS CN1-00393).

The identified colonies presented a typical red-orange cenosarc. The first colony had a total of 64 yellowish polyps measuring 75.45 mm in average length, 60.21 mm in average width, 44.40 mm in average height, as 3.92 mm and 5.67 mm in average height and diameter of corallite, respectively (Table 2). The other colony had a total of 17 yellowish polyps measuring 32.62 mm in average length, 29.38 mm in average width, 17.28 mm in average height, as 2.56 mm and 5.66 mm in average height and diameter of corallite, respectively (Table 2). As they presented little-to-no spacing between corallites, nor budding from them, as well as other characteristics, the coral colonies are identified as Tubastraea coccinea Lesson, 1830.

Table 2.
Linear measurements (mm) of Tubastraea coccinea recorded in the Vaza-Barris River estuary.

Tubastraea	Length	Width	Height	Height of coralite	Diameter of corallite
Colony 1	75.45	60.21	44.40	0.90–6.05	3.39–8.47
Colony 2	32.62	29.38	17.28	0.97–5.07	2.51–7.87

Discussion

These onshore records of the invasive coral T. coccinea extend its distribution in the state of Sergipe to the coastal region, as previous occurrences were limited to the continental shelf on oil production platforms approximately 13 km offshore. Contaminated oil platforms and vessels can be vectors, functioning as stepping-stones that connect oceanic regions to the coast (Costa et al. 2014), as there are records of vessels that make the offshore-onshore route which anchor close the detection site. Another possible route of contamination would be the dispersion of planulae by sea currents responsible for transporting larvae and allowing the colonization of new areas (Dottori et al. 2018). Despite presenting a long-lasting larval stage (Coelho et al. 2022), this would be a less likely hypothesis because of the fragility of its larvae and their tendency to establish themselves close to the parental colonies (Creed et al. 2017).

Two species of Tubastraea have invaded the South Atlantic, T. coccinea and T. tagusensis (Creed et al. 2017), although the taxonomy of Tubastraea is under constant review. For example, evidence in Brazil of a third species, a morphological clade with an intermediate morphology, has been presented but was rejected by molecular analyses (Bastos et al. 2022) and considered to be T. coccinea. As the colony described here has this intermediate morphology [compare Figure. 2 with Bastos et al. (2022) Figure 2, p.194], based on current evidence we consider it to be T. coccinea. Interestingly, all three morphotypes (T. coccinea, T. tagusensis, and Tubastraea sp.) have been reported on nearby offshore platforms (Petrobras, 2016). Tubastraea coccinea (summing Tubastraea sp.) is more frequent (88%) and abundant in substratum occupation (density of T. coccinea intersection points, mean of all platforms = 116) than T. tagusensis (77% and density of intersection points, mean of all platforms = 32 respectively; data from ANEXO A-VI.2.1-1, Petrobras, 2016), suggesting the propagule pressure from the offshore platforms is four times greater for T. coccinea than for T. tagusensis.

Invasive characteristics, such as high reproductive rate, hermaphroditism, high dispersion capacity (De Paula et al. 2014), resistance to temperature and salinity variations (Moreira et al. 2014, Almeida Saá et al. 2020), as well as plasticity regarding the fouling substrate (Silva et al. 2022), explain the establishment and continuous advance of the species across the most diverse environments. On the Brazilian coast, its invasion extends along more that at least 3,000 km of coastline (Meurer et al. 2010, Soares-Gomes et al. 2016), altering trophic relationships and the realized niches of native species, leading to a decline in local richness and loss of diversity (Silva et al. 2023). Studies have shown that an increase in Tubastraea populations in native communities can result in drastic reductions in the main groups of invertebrates, such as copepods, ostracods, and tanaids (Silva et al. 2019), which are important food sources for the larval stages of fish. Considering the richness and ecological importance of bivalves on the coast of Sergipe, as well as their positive relationship with macroalgae (Santos et al. 2020), the presence and subsequent advancement of sun coral may represent an inherent threat to these groups.

The propagule pressure caused by the continuous transit of contaminated vessels from offshore platforms to estuaries increases the chances of sun coral establishment and invasion (Castro et al. 2021). Another relevant factor is represented by the growing number of artificial structures in the region resulting from coastal urbanization driven by changes in coastal infrastructure, shipping, tourism, and recreation, leading to the disturbance of native communities, and the provision of conditions that facilitate invasion (Dodds et al. 2022); artificial substrates have been shown to better facilitate Tubastraea spp. than natural substrates (Mangelli & Creed 2012). Likewise, further dispersal of the genus Tubastraea to other locations in the Vaza-Barris River estuary may be favored by the frequent traffic of private and tourist vessels (Tempesti et al. 2022) and by the seawater intrusion in the region, a condition observed by Miranda et al. (2016) in the Baía de Todos os Santos.

The syntopic benthic community in the Vaza-Barris estuary includes native (e.g. oysters, crustaceans, and hydrozoans) (Mendonça et al. 2022) and non-native invertebrates (e.g. Lysmata lipkei and L. vittata) (Alves et al. 2018). In the dives that preceded the removal of Tubastraea, we observed Menippe nodifrons associated with the colony that subsequently disappeared from the site. This relationship between brachyuran crabs and sun coral colonies is classified as occasional (Silva et al. 2023), because they use different biogenic substrates throughout their life history (Barros-Alves et al. 2018). Its association with Tubastraea suggests that it provides favorable conditions for structural complexity and feeding. Other non-native species may also benefit from this association with sun coral.

Conclusion

The record of T. coccinea in the coastal zone of the state of Sergipe, in addition to expanding the occurrence of the genus in Brazil, raises an alert for the possible expansion of the species throughout the estuarine complex of the Vaza-Barris River and other estuaries in the state as well as along the coast. The size of the largest colony suggests it was 8 years old (based on known growth rates of increment of 8 polyps.yr^-1 and 0.92 cm.yr^-1 in colony width, De Paula (2007), but no founding polyps were observed on substrates nearby which is not usually the case, so local conditions may not allow reproduction. The removals may be considered control actions, and thus, the site should be monitored over time to determine if the eradication was 100% effective. Considering the importance of these systems for the maintenance of native communities and the impacts of the invasion of exotic species, the detection of sun coral signals the urgency for public managers to perform action plans and constant monitoring to reduce the damage caused by this invasive coral. Public policy must be implemented to repress the commercialization of sun coral in Sergipe, which already occurs on social media.

Acknowledgments

We thank funding from Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro [grant numbers FAPERJ E-26/010.003031/2014 and E26/203.002/2017 (JCC)] and Conselho Nacional de Desenvolvimento Científico e Tecnológico [grant numbers 312779/2021-6 (MFGB), 313698/2021-0 (JCC)]. This article is no. 55 from the Projeto Coral-Sol.

Data Availability

Supporting data are available at https://figshare.com/s/7e63efeb44fc6723992c

References

• ALMEIDA SAÁ, A.C., CRIVELLARO, M.S., WINTER, B.B., PEREIRA, G.R., BERCOVICH, M.V., HORTA, P.A., BASTOS, E.O. & SCHUBERT, N. 2020. Unraveling interactions: do temperature and competition with native species affect the performance of the non-indigenous sun coral Tubastraea coccinea?. Coral Reefs, 39(1), 99–117. https://doi.org/10.1007/s00338-019-01870-0.
  » https://doi.org/10.1007/s00338-019-01870-0
• ALVES, D.F.R., LIMA, D.J.M., HIROSE, G.L., MARTINEZ, P.A., DOLABELLA, S.S. & BARROS-ALVES, S.P. 2018. Morphological and molecular analyses confirm the occurrence of two sympatric Lysmata shrimp (Crustacea, Decapoda) in the southwestern Atlantic. Zootaxa, 4526(1), 41–55. https://doi.org/10.11646/zootaxa.4526.1.3.
  » https://doi.org/10.11646/zootaxa.4526.1.3
• BARROS-ALVES, S.P., ALVES, D.F.R. & COBO, V. J. 2018. Brachyuran crab (Crustacea, Decapoda) assemblage associated with Sargassum cymosum in southeastern Brazil. Marine Biodiversity, 48(4), 2043–2055. https://doi.org/10.1007/s12526-017-0730-3.
  » https://doi.org/10.1007/s12526-017-0730-3
• BASTOS, N., CALAZANS, S.H., ALTVATER, L., NEVES, E.G., TRUJILLO, A.L., SHARP, W.C., HOFFMAN, E.A. & COUTINHO R. 2022. Western Atlantic invasion of sun corals: incongruence between morphology and genetic delimitation among morphotypes in the genus Tubastraea Bulletin of Marine Science. 98(2), 187–210. https://doi.org/10.5343/bms.2021.0031.
  » https://doi.org/10.5343/bms.2021.0031
• BROCKINTON, E.E., PETERSON, M.R., WANG, H.H. & GRANT, W.E. 2022. Importance of Anthropogenic Determinants of Tubastraea coccinea invasion in the Northern Gulf of Mexico. Water (Switzerland), 14(9). https://doi.org/10.3390/w14091365.
  » https://doi.org/10.3390/w14091365
• CAIRNS, S.D. 1991. A revision of the ahermatypic scleractinia of the Galápagos and Cocos islands. Smith. Contr. Zool, 504: 1–56.
• CAPEL, K.C.C., CREED, J.C., KITAHARA, M.V., CHEN, C.A. & ZILBERBERG, C. 2019. Multiple introductions and secondary dispersion of Tubastraea spp. in the Southwestern Atlantic. Scientific Reports, 9(1). https://doi.org/10.1038/s41598-019-50442-3.
  » https://doi.org/10.1038/s41598-019-50442-3
• CASTRO, C.B. & PIRES, D.O. 2001. Brazilian coral reefs: what we already know and what is still missing. Bull. Mar. Sci. 69, 357–371.
• CASTRO, N., RAMALHOSA, P., CACABELOS, E., COSTA, J.L., CANNING-CLODE, J. & GESTOSO, I. 2021. Winners and losers: prevalence of non-indigenous species under simulated marine heatwaves and high propagule pressure. Marine Ecology Progress Series, 668, 21–38. https://doi.org/10.3354/meps13710.
  » https://doi.org/10.3354/meps13710
• COELHO, S.C.C., GHERARDI, D.F.M., GOUVEIA, M.B. & KITAHARA, M.V. 2022. Western boundary currents drive sun-coral (Tubastraea spp.) coastal invasion from oil platforms. Scientific Reports, 12(1). https://doi.org/10.1038/s41598-022-09269-8.
  » https://doi.org/10.1038/s41598-022-09269-8
• COSTA, T.J.F., PINHEIRO, H.T., TEIXEIRA, J.B., MAZZEI, E.F., BUENO, L., HORA, M.S.C., JOYEUX, J.C., CARVALHO-FILHO, A., AMADO-FILHO, G., SAMPAIO, C.L.S. & ROCHA, L.A. 2014. Expansion of an invasive coral species over Abrolhos Bank, Southwestern Atlantic. Marine Pollution Bulletin, 85(1), 252–253. https://doi.org/10.1016/j.marpolbul.2014.06.002.
  » https://doi.org/10.1016/j.marpolbul.2014.06.002
• CREED, J.C., FENNER, D., SAMMARCO, P., CAIRNS, S., CAPEL, K., JUNQUEIRA, A.O.R., CRUZ, I., MIRANDA, R.J, CARLOS-JUNIOR, L., MANTELATTO, M.C. & OIGMAN-PSZCZOL, S. 2017. The invasion of the azooxanthellate coral Tubastraea (Scleractinia: Dendrophylliidae) throughout the world: history, pathways and vectors. In Biological Invasions. Springer International Publishing, 19(1), 283–305. https://doi.org/10.1007/s10530-016-1279-y.
  » https://doi.org/10.1007/s10530-016-1279-y
• DE PAULA, A.F. 2007. Biologia reprodutiva, crescimento e competição dos corais invasores Tubastraea coccinea e Tubastraea tagusensis (Scleractinia: Dendrophyllidae) com espécies nativas. PhD Thesis, Museu Nacional, Universidade Federal do Rio de Janeiro, Rio de Janeiro: 108 p.
• DE PAULA, A.F., DE OLIVEIRA PIRES, D. & CREED, J.C. 2014. Reproductive strategies of two invasive sun corals (Tubastraea spp.) in the southwestern Atlantic. Journal of the Marine Biological Association of the United Kingdom, 94(3), 481–492. https://doi.org/10.1017/S0025315413001446.
  » https://doi.org/10.1017/S0025315413001446
• DE PAULA, F.A. & CREED, J.C. 2004. Two species of the coral Tubastraea (cnidaria, scleractinia) in brazil: a case of accidental introduction. In bulletin of marine Science,74(1).
• DEROUEN, Z.C., PETERSON, M.R., WANG, H.H. & GRANT, W.E. 2020. Determinants of Tubastraea coccinea invasion and likelihood of further expansion in the northern Gulf of Mexico. Marine Biodiversity, 50, 1–11. https://doi.org/10.1007/s12526-020.
  » https://doi.org/10.1007/s12526-020
• DIAGNE, C., LEROY, B., VAISSIÈRE, A.C., GOZLAN, R.E., ROIZ, D., JARIĆ, I., SALLES, J.M., BRADSHAW, C.J.A. & COURCHAMP, F. 2021. High and rising economic costs of biological invasions worldwide. Nature, 592(7855), 571–576. https://doi.org/10.1038/s41586-021-03405-6.
  » https://doi.org/10.1038/s41586-021-03405-6
• DODDS, K.C., SCHAEFER, N., BISHOP, M.J., NAKAGAWA, S., BROOKS, P.R., KNIGHTS, A.M. & STRAIN, E.M.A. 2022. Material type influences the abundance but not richness of colonising organisms on marine structures. Journal of Environmental Management, 307. https://doi.org/10.1016/j.jenvman.2022.114549.
  » https://doi.org/10.1016/j.jenvman.2022.114549
• DOTTORI, M., SILVEIRA, I.C.A., CASTRO-FILHO, B.M., BRAGA, E.S., DOTTORI, F.R., WATANABE, W.B., BALDASSO, P., BERBEL, G.B.B. & NAPOLITANO, D.C. 2018. Física: Caracterização de correntes e assas d’água oceânicas na bacia Sergipe-alagoas. Revista MARSEAL, Águas profundas SE/AL. São Cristóvão, SE. 22–39.
• FERRARIO, J., CARONNI, S., OCCHIPINTI-AMBROGI, A. & MARCHINI, A. 2017. Role of commercial harbours and recreational marinas in the spread of non-indigenous fouling species. Biofouling, 33(8), 651–660. https://doi.org/10.1080/08927014.2017.1351958.
  » https://doi.org/10.1080/08927014.2017.1351958
• HARDOIM, C.C.P., RAMAGLIA, A.C.M., LÔBO-HAJDU, G. & CUSTÓDIO, M.R. 2021. Community composition and functional prediction of prokaryotes associated with sympatric sponge species of southwestern Atlantic coast. Scientific Reports, 11(1). https://doi.org/10.1038/s41598-021-88288-3.
  » https://doi.org/10.1038/s41598-021-88288-3
• HEWITT, C.L., GOLLASCH, S. & MINCHIN, D. 2009. The vessel as a vector–biofouling, ballast water and sediments. In Biological invasions in marine ecosystems: Ecological, management, and geographic perspectives. Berlin, Heidelberg: Springer Berlin Heidelberg, 117–131.
• HULME, P.E. 2021. Unwelcome exchange: International trade as a direct and indirect driver of biological invasions worldwide. In One Earth, 4(5) 666–679). https://doi.org/10.1016/j.oneear.2021.04.015.
  » https://doi.org/10.1016/j.oneear.2021.04.015
• LAGES, B.G., FLEURY, B.G., MENEGOLA, C. & CREED, J.C. 2011. Change in tropical rocky shore communities due to an alien coral invasion. Marine Ecology Progress Series, 438, 85–96. http://dx.doi.org/10.3354/meps09290.
  » https://doi.org/10.3354/meps09290
• LEMOS JUNIOR, I.C., MACHADO, A.J., ANDRADE, E.J., VIEIRA, F.S. & GUIMARÃES, C.R.P. 2014. Macroforaminíferos da plataforma continental de Sergipe, Brasil. Scientia plena, 10(10).
• LÓPEZ, C., CLEMENTE, S., MORENO, S., OCAÑA, O., HERRERA, R., MORO, L., MONTERROSO, O., RODRÍGUEZ, A. & BRITO, A. 2019. Invasive Tubastraea spp. and Oculina patagonica and other introduced scleractinians corals in the Santa Cruz de Tenerife (Canary Islands) harbor: Ecology and potential risks. Regional Studies in Marine Science, 29. https://doi.org/10.1016/j.rsma.2019.100713.
  » https://doi.org/10.1016/j.rsma.2019.100713
• LOWEN, J.B. & DIBACCO, C. 2023. Range expansion and establishment of a non-indigenous tunicate (Diplosoma listerianum) in thermal refugia is mediated by environmental variability in changing coastal environments. Canadian Journal of Fisheries and Aquatic Sciences, 80(2), 330–345. https://doi.org/10.1139/cjfas-2022-0082.
  » https://doi.org/10.1139/cjfas-2022-0082
• MABROUKI, Y., CROCETTA, F. & TAYBI, A.F. 2021. First Record of Branchiomma luctuosum (Grube, 1870) (Annelida: Polychaeta: Sabellidae) in Morocco. Thalassas, 37(2), 717–720. https://doi.org/10.1007/s41208-021-00348-7.
  » https://doi.org/10.1007/s41208-021-00348-7
• MANGELLI, T.S. & CREED, J.C. 2012. Análise comparativa da abundância do coral invasor Tubastraea spp: (Cnidaria, Anthozoa) em substratos naturais e artificiais na Ilha Grande, Rio de Janeiro, Brasil. Iheringia Série Zoologia, 102: p. 122–130.
• MARKS, L.M., REED, D.C. & HOLBROOK, S.J. 2020. Niche Complementarity and resistance to grazing promote the invasion success of Sargassum horneri in North America. Diversity, 12(2). https://doi.org/10.3390/d12020054.
  » https://doi.org/10.3390/d12020054
• MENDONÇA, L.M.C., GUIMARÃES, C.R.P. & HADDAD, M.A. 2022. Taxonomy and diversity of hydroids (Cnidaria: Hydrozoa) of Sergipe, Northeast Brazil. Zoologia, 39, e21032. https://doi.org/10.1590/S1984-4689.v39.e21032.
  » https://doi.org/10.1590/S1984-4689.v39.e21032
• MEURER, B.C., LAGES, N.S., PEREIRA, O.A., PALHANO, S. & MAGALHÃES, G.M. 2010. First record of native species of sponge overgrowing invasive corals Tubastraea coccinea and Tubastraea tagusensis in Brazil. Marine Biodiversity Records. 3. https://doi.org/10.1017/s1755267210000527.
  » https://doi.org/10.1017/s1755267210000527
• MIRANDA, R.J., COSTA, Y., LORDERS, F.L., DE ANCHIETA, C.C. & BARROS, F. 2016. New records of the alien cup-corals (Tubastraea spp.) within estuarine and reef systems in Todos os Santos Bay, Southwestern Atlantic. Marine Biodiversity Records. 9(1). https://doi.org/10.1186/s41200-016-0053-2.
  » https://doi.org/10.1186/s41200-016-0053-2
• MIRANDA, R. J., TAGLIAFICO, A., KELAHER, B.P., MARIANO-NETO, E. & BARROS, F. 2018. Impact of invasive corals Tubastraea spp. on native coral recruitment. Marine Ecology Progress Series, 605, 125–133. https://doi.org/10.3354/meps12731.
  » https://doi.org/10.3354/meps12731
• MIRANDA, R.J., NUNES, J.A.C.C., CREED, J.C., BARROS, F., MACIEIRA, R.M., SANTOS, R.G., LIMA, G.V., PONTES, A.V.F., SILVA, L.G.F.C., CORDEIRO, R.T., SAMPAIO, C.L.S., PINTO, T.K., MALHADO, A.C.M., LADLE, R. & PEREIRA, P.H.C. 2020. Brazil policy invites marine invasive species. Association for the Advancement of Science, 368(6490), 481. American. https://doi.org/10.1126/science.abb7255.
  » https://doi.org/10.1126/science.abb7255
• MIRANDA, R.J., PINTO, T.K.O., LOPES, R.V.R., SANTOS, J.W., SAMPAIO, C.L.S., SANTOS, R.G., PEREIRA, P.H.C., CARDOSO, A.T.C., MALHADO, A.C.M. & LADLE, R.J. 2022. Oil Spill Disaster in Southwest Atlantic Coast: an Evaluation of Short-Term Effects on Coral Reef Benthic Assemblages. Anais Da Academia Brasileira de Ciencias, 94. https://doi.org/10.1590/0001-3765202220210401.
  » https://doi.org/10.1590/0001-3765202220210401
• MOREIRA, P.L., RIBEIRO, F.V. & CREED, J.C. 2014. Control of invasive marine invertebrates: an experimental evaluation of the use of low salinity for managing pest corals (Tubastraea spp.). Biofouling, 30(5), 639–650. https://doi.org/10.1080/08927014.2014.906583.
  » https://doi.org/10.1080/08927014.2014.906583
• OLIVEIRA, L.S. & SOUZA, R.M. 2015. Estuarine morphodynamics and variations of the ebb-tidal delta in the Vaza-barris river, SE, Brazil. Revista Brasileira de Geomorfologia, 16, 4.
• PETROBRAS. 2016. Projeto de Avaliação da Bioincrustação pelo Coral-sol nas Instalações da Petrobras no Litoral de Sergipe. In: Junior SdS, Rita CdS (eds). Unidade de Operações de Exploração e Produção de Sergipe-Alagoas (UOSEAL), Petrobras, 139.
• QGIS.org. 2023. QGIS 3.28.3. Geographic Information System. QGIS Association. http://www.qgis.org
  » http://www.qgis.org
• SAMPAIO, C.L., MIRANDA, R.J., MAIA-NOGUEIRA, R. & JOSÉ DE ANCHIETA, C.C. 2012. New occurrences of the nonindigenous orange cup corals Tubastraea coccinea and T tagusensis (Scleractinia: Dendrophylliidae) in Southwestern Atlantic. Check List, 8(3), 528–530. https://doi.org/10.15560/8.3.528.
  » https://doi.org/10.15560/8.3.528
• SANTOS, H.S., BERTOLLO, J.C. & CREED, J.C. 2023. Range extension of the Asian green mussel Perna viridis (Linnaeus, 1758) into a Marine Extractive Reserve in Brazil. BioInvasions Records, 12(1), 208–222. https://doi.org/10.3391/bir.2023.12.1.17.
  » https://doi.org/10.3391/bir.2023.12.1.17
• SANTOS, L., WEVERTON, J., SOUZA, S., LIMA, S. & GUIMARÃES, C. 2020. Diversity of Bivalve Mollusks Associated with Macroalgae on the Continental Shelf in the States of Alagoas, Sergipe and Bahia, Northeastern Brazil. Zoological studies, 59. https://doi.org/10.6620/ZS.2020.59-58.
  » https://doi.org/10.6620/ZS.2020.59-58
• SANTOS, L.A. & LATRUBESSE, E.M. 2022. The Vaza-Barris River: A late Quaternary decoupled accumulation-erosion model for rivers of the NE Brazil Atlantic passive margin. Journal of South American Earth Sciences, 120. https://doi.org/10.1016/j.jsames.2022.104077.
  » https://doi.org/10.1016/j.jsames.2022.104077
• SHIGANOVA, T.A., SOMMER U., JAVIDPOUR J., MOLINERO J.C., MALEJ A., KAZMIN A.S., ISINIBILIR M., CHRISTOU E., SIOKOU-FRANGOU I., MARAMBIO M., FUENTES V., MIRSOYAN Z.A., GÜLSAHIN N., LOMBARD F., LILLEY M.K.S., ANGEL D.L., GALIL B.S., BONNET D. & DELPY F. 2019. Patterns of invasive ctenophore Mnemiopsis leidyi distribution and variability in different recipient environments of the Eurasian seas: A review. Marine Environmental Research, 152, 104791. https://doi.org/10.1016/j.marenvres.2019.104791.
  » https://doi.org/10.1016/j.marenvres.2019.104791
• SILVA, A.G., DE PAULA, A.F., FLEURY, B.G. & CREED, J.C. 2014. Eleven years of range expansion of two invasive corals (Tubastraea coccinea and Tubastraea tagusensis) through the southwest Atlantic (Brazil). Estuarine, Coastal and Shelf Science. 141, 9–16. https://doi.org/10.1016/j.ecss.2014.01.013.
  » https://doi.org/10.1016/j.ecss.2014.01.013
• SILVA, A.R, CREED, J.C. & TAVARES, M. 2023. Species diversity and abundance of mobile crustaceans associated with living and dead colonies of the invasive sun coral Tubastraea Aquatic Ecology, 57(2), 529–541. https://doi.org/10.1007/s10452-023-10027-9.
  » https://doi.org/10.1007/s10452-023-10027-9
• SILVA, M.S., DE MORAES, F.C., BATISTA, D., BAHIA, R.G., BERTONCINI, Á.A., MACHADO, A.A., MURICY, G., KAREZ, C.S., PEREIRA-FILHO, G.H., SALGADO, L.T. & PEREIRA, R.C. 2022. Distribution, population structure and settlement preference of Tubastraea spp. (Cnidaria: Scleractinia) on rocky shores of the Cagarras Islands Natural Monument and surroundings, Rio de Janeiro, Brazil. Regional Studies in Marine Science, 52. https://doi.org/10.1016/j.rsma.2022.102245.
  » https://doi.org/10.1016/j.rsma.2022.102245
• SILVA, R., VINAGRE, C., KITAHARA, M.V., ACORSI, I.V., MIZRAHI, D. & FLORES, A.A. 2019. Sun coral invasion of shallow rocky reefs: effects on mobile invertebrate assemblages in Southeastern Brazil. Biological Invasions, 21, 1339–1350. https://doi.org/10.1007/s10530-018-1903-0.
  » https://doi.org/10.1007/s10530-018-1903-0
• SOARES, E.C., BISPO, M.D, VASCONCELOS, V.C., SOLETTI, J.I., CARVALHO, S.H.V., OLIVEIRA, M.J., SANTOS, M.C., SANTOS FREIRE, E., NOGUEIRA, A.S.P., SILVA CUNHA, F.A., SANDES, R.D.D., SANTOS, R.A.R., NETA, M.T.S.L., NARAIN, N., GARCIA, C.A.B., COSTA, S.S.L. & SANTOS, J.C.C. 2021. Oil impact on the environment and aquatic organisms on the coasts of the states of Alagoas and Sergipe, Brazil – A preliminary evaluation. Marine Pollution Bulletin, 171. https://doi.org/10.1016/j.marpolbul.2021.112723.
  » https://doi.org/10.1016/j.marpolbul.2021.112723
• SOARES-GOMES, A., GAMA, B.A.P, BAPTISTA NETO, J.A., FREIRE, D.G., CORDEIRO, R.C., MACHADO, W., BERNARDES, M.C., COUTINHO, R, THOMPSON, F.L. & PEREIRA, R.C. 2016. An environmental overview of Guanabara Bay, Rio de Janeiro. Regional Studies in Marine Science, 8, 319–330. https://doi.org/10.1016/j.rsma.2016.01.009.
  » https://doi.org/10.1016/j.rsma.2016.01.009
• SOARES, M.O., DAVIS, M. & DE MACÊDO CARNEIRO, P.B. 2018. Northward range expansion of the invasive coral (Tubastraea tagusensis) in the southwestern Atlantic. Marine Biodiversity, 48(3), 1651–1654. https://doi.org/10.1007/s12526-016-0623-x.
  » https://doi.org/10.1007/s12526-016-0623-x
• TEMPESTI, J., LANGENECK, J., ROMANI, L., GARRIDO, M., LARDICCI, C., MALTAGLIATI, F. & CASTELLI, A. 2022. Harbour type and use destination shape fouling community and non-indigenous species assemblage: A study of three northern Tyrrhenian port systems (Mediterranean Sea). Marine Pollution Bulletin, 174. https://doi.org/10.1016/j.marpolbul.2021.113191.
  » https://doi.org/10.1016/j.marpolbul.2021.113191
• WANG, C., XU, M., ZHANG, J. & ZHOU, X. 2024. High-latitude invasion and environmental adaptability of the freshwater mussel Limnoperna fortunei in Beijing, China. Ecological Applications, 34(1). https://doi.org/10.1002/eap.2887.
  » https://doi.org/10.1002/eap.2887

Edited by

• Associate Editor
  Tito Lotufo

Publication Dates

• Publication in this collection
  18 Oct 2024
• Date of issue
  2024

History

• Received
  12 Apr 2024
• Accepted
  13 Sept 2024