Introduction
The introduction of non-native species in marine and coastal ecosystems due to human activity can cause extinction of native populations, destroy biodiversity, permanently alter habitats and have economic impacts, leading to fundamental disruptions of the aquatic ecosystems (Ojaveer et al., Reference Ojaveer, Galil, Carlton, Alleway, Goulletquer, Lehtiniemi and Zaiko2018; Vitule et al., Reference Vitule, Occhi, Kang, Matsuzaki, Bezerra, Daga and Padial2019). The establishment of non-native populations depends on a species' ability to adapt to new environmental forces, produce fertile offspring, and disperse recruits into the new environment (Richardson et al., Reference Richardson, Pysek, Rejmánek, Barbour, Panetta and West2000; Wonham et al., Reference Wonham, Carlton, Smith and College2000; Olenin et al., Reference Olenin, Gollasch, Lehtiniemi, Sapota, Zaiko and Snoeijs-Leijonmalm2017). The number of registered non-native species has increased in marine and coastal environments (Tempesti et al., Reference Tempesti, Mangano, Langeneck, Lardicci, Maltagliati and Castelli2020; Encarnação et al., Reference Encarnação, Teodósio and Morais2021). The increase of introduced species has also been documented in the Southwestern Atlantic and along the Brazilian Coast since the mid-2000s (Schwindt et al., Reference Schwindt, Carlton, Orensanz, Scarabino and Bortolus2020). Many of these non-native species exhibit a benthic cryptic behaviour, such as species in the families Gobiidae and Blenniidae (Ferreira et al., Reference Ferreira, Junqueira, Villac, Lopes, Rilov and Crooks2009).
The family Blenniidae is comprised of approximately 360 species across 56 genera, distributed in tropical and subtropical marine and estuarine habitats such as tide pools, rocky shores, mangroves, and salt marshes (Nelson, Reference Nelson2006). The muzzled blenny Omobranchus sewalli (Valenciennes, 1836) reaches 11 cm long with males typically larger than females, has a short life span (ca. 4 years) and feeds on algae and opportunistically on invertebrates (Ismail and Clayton, Reference Ismail and Clayton1990). Additionally, their cryptic, sedentary, and territorial behaviour, oviparity and high parental care may directly affect the niche of native gobies and blennies (Ismail and Clayton, Reference Ismail and Clayton1990; Gerhardinger et al., Reference Gerhardinger, Freitas, Andrade and Rangel2006; Froese and Pauly, Reference Froese and Pauly2023). This species was registered as invasive in 1931 on the coast of Trinidad and Tobago (Cervigon, Reference Cervigon1966). Afterwards, several specimens were collected in Panama and Venezuela (Cabezas et al., Reference Cabezas, Lasso-Alcalá, Xavier and Jowers2020). In Brazil, O. sewalli was initially recorded under O. punctatus in 2002 on the Northeast coast (Gerhardinger et al., Reference Gerhardinger, Freitas, Andrade and Rangel2006), and from 2004 to 2014 registered in the Southeast and South of Brazil (Cabezas et al., Reference Cabezas, Lasso-Alcalá, Quintero, Xavier, Giarrizzo, Nunes, Machado, Gómez, Silva Pedroza and Jowers2022). The integrative taxonomy showed the occurrence of Omobrancus sewalli in the Western Atlantic Ocean and not Omobranchus punctatus using meristic and genetic data from specimens from the Caribbean, Northern and Northeastern Brazil (Cabezas et al., Reference Cabezas, Lasso-Alcalá, Quintero, Xavier, Giarrizzo, Nunes, Machado, Gómez, Silva Pedroza and Jowers2022). In the present study we report the first record of mature adults of O. sewalli within the Paranaguá Estuarine Complex (PEC), a World Natural Heritage Site (UNESCO, 1999) and a recognized RAMSAR site, making it part of the List of Wetlands of International Importance (ICMBio, 2018; Ribeiro et al., Reference Ribeiro, Moura, Stenert, Florín and Maltchik2020). Herein, we also show the application of fish-specific autonomous reef monitoring structures (FARMS) (Brandl et al., Reference Brandl, Weigt, Pitassy, Coker, Patrick, Luchese, Berumen, Buskey, Casey, Di Domenico, Soeth, Topor, Duffy, Baldwin, Hagedorn and Parenti2023) monitoring invasive cryptobenthic fishes.
Materials and Methods
Ethical statement
The capture of all specimens complied with animal welfare laws, guidelines and policies, approved by the national licensing authority the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA) with licence number 87398 and Ethics Committee of Federal University of Paraná number 1561.
Study sites and data acquisition
The Paranaguá Estuarine Complex (PEC – 25°26′ 43′′S 48° 39′ 58′′W, Figure 1), with an area of ~551.8 km2, is a subtropical environment composed of mangroves, salt marshes, and shallow waters. Salinity and temperature vary seasonally from 0 to 32 g l−1 and from 18–30°C, respectively (Lessa et al., Reference Lessa, Santos, Filho, Corrêa-Gomes, Lana and Bernardino2018). It has a mosaic of restricted and sustainable-use conservation units, including marine and terrestrial units (Paula et al., Reference Paula, Pigosso and Wroblewski2018). In addition, it houses two ports on the East–West axis, the port of Antonina and the port of Paranaguá, considered one of Brazil's largest grain ports in South America with one of the largest port infrastructures on the continent (Marone et al., Reference Marone, Machado, Lopes and Da Silva2005).
Figure 1. (A) Sampling sites of Omobranchus sewalli in the Paranaguá Estuarine Complex in the Subtropical Southwestern Atlantic Ocean. The number refers to the sampling site: (1) Amparo village community and (2) São Miguel village. The ship symbols indicate the position of the Antonina and Paranaguá Port. (B) FARMS deployed in Amparo Village, (C) FARMS deployed in São Miguel Village, (D) Photographs of captured specimens in São Miguel in November 2023.
Five FARMS were installed in August 2023 (winter) among rocky shore area in the Amparo and São Miguel communities with the contribution of the local students. The FARMS were built according to Brandl et al. (Reference Brandl, Weigt, Pitassy, Coker, Patrick, Luchese, Berumen, Buskey, Casey, Di Domenico, Soeth, Topor, Duffy, Baldwin, Hagedorn and Parenti2023). Two fishing campaigns were carried out, one in the first week of October 2023 (early spring) and the second in the last week of November 2023 (late spring). Specimens were identified (Williams, Reference Williams and Carpenter2002; Rangel and Guimarães, Reference Rangel and Guimarães2010), measured for total length (TL, cm) and weighed (TW, total weight in grams). The table of meristic characters was created according to Williams (Reference Williams and Carpenter2002) and Cabezas et al. (Reference Cabezas, Lasso-Alcalá, Quintero, Xavier, Giarrizzo, Nunes, Machado, Gómez, Silva Pedroza and Jowers2022). The sex and maturation stage of the specimens was macroscopically verified according to Vazzoler (Reference Vazzoler1996). We measured the environmental parameters of salinity (g l−1) and water temperature (°C) in the site.
Results
A total of five specimens were collected after one month and two months of FARMS were installed. The specimens analysed presented two interorbital pores, between 29 and 33 total dorsal fin elements, between 13 and 14 rays in the pectoral fin and between 12 and 14 rays in the caudal fin. Four specimens of O. sewalli were collected in October 2023 and ranged from 5.6 to 8.5 cm (TL), and 1.46–4.72 g (TW). One specimen was collected in November 2023 (Table 1). In October, the water temperature in Amparo and São Miguel was 20°C and the salinity was 28 g l−1 in Amparo and 32 g l−1 in São Miguel. The water temperature in São Miguel was 27.8°C in November 2023. Other species associated with O. sewalli in the FARMs were the fishes Bathygobius soporator, Orthopristis ruber, Parablenius pilicornis, and Opsanus beta and several other invertebrates as Pseudobranchiomma paulista.
Table 1. Total length (TL, cm), weight (TW, g), female (F) and male (M), and stage of maturation of specimens of Omobranchus sewali by site collected in Paranaguá Estuarine Complex, south Brazil
Discussion
In the present study, Omobranchus sewalli was reported for the first time within the PEC. The population expansion into the estuary may be a natural dispersal or facilitated by human activities. Omobranchus sewalli was first introduced to the Western Atlantic Ocean on slave boats from the Bay of Bengal (Cervigon, Reference Cervigon1966) and now has been recorded in several regions along the Brazilian coast (Cabezas et al., Reference Cabezas, Lasso-Alcalá, Quintero, Xavier, Giarrizzo, Nunes, Machado, Gómez, Silva Pedroza and Jowers2022), reinforcing the hypothesis that colonization of new environments by introduced species is facilitated by the dispersal of pelagic larvae (Wonham et al., Reference Wonham, Carlton, Smith and College2000). Omobranchus sewalli larvae were recorded in Babitonga Bay (SC) between 2004 and 2008 and in Currais Archipelago (near 16 km from the mouth of the PEC – PR) between 2011 and 2012 (Costa et al., Reference Costa, Souza-Conceição, Schwingel and Spach2011; Alegretti et al., Reference Alegretti, Grande, Namiki, Loose and Brandini2021). The population of O. sewalli in PEC may have been established by the settlement of larvae transported by longitudinal drift (or tide) currents from the Currais Archipelago into the PEC. This process of establishing new populations via longitudinal drift has also occurred in the Caribbean Sea (Lasso-Alcalá et al., Reference Lasso-Alcalá, Nunes, Lasso, Posada, Robertson, Piorski, Tassell, Giarrizzo and Gondolo2011).
The occurrence of the O. sewalli in Amparo and São Miguel villages in front of the Paranaguá Port also emphasizes the hypothesis of species introduction through ballast water and fouling on the ship hull (Lasso-Alcalá et al., Reference Lasso-Alcalá, Nunes, Lasso, Posada, Robertson, Piorski, Tassell, Giarrizzo and Gondolo2011). Along the Brazilian coast, the cabotage service is responsible for transporting products between ports in the Southeast-South regions, and the Brazilian legislation does not determine as mandatory the disposal of maritime cabotage service ballast water in oceanic areas before docking at ports (NORMAM, 2014; Cutrim et al., Reference Cutrim, Robles, Galvão and Casaca2017). Therefore, the presence of larvae and juveniles of O. sewalli can be dispersed by ballast water, favouring the establishment of population in new environments such as the PEC. Also, O. sewalli has been frequently associated with fouling communities of artificial structures, such as boats and aquaculture fish cages, and natural substrates, such as under rocks in tidal pools. Most of these are located near major ports and seaways (Lasso-Alcalá et al., Reference Lasso-Alcalá, Nunes, Lasso, Posada, Robertson, Piorski, Tassell, Giarrizzo and Gondolo2011). Considering the behaviour and preferred habitat of this species, another hypothesis for the dispersion of O. sewalli is their use of using mollusc valves for spawning. During the benthic phase of the larvae, they can be dispersed due to their attachment to fouling organisms by commercial transport ships (Lasso-Alcalá et al., Reference Lasso-Alcalá, Nunes, Lasso, Posada, Robertson, Piorski, Tassell, Giarrizzo and Gondolo2011).
Since the mature specimens indicate an established population in the mixture zone of PEC together with the native community of fish, it is imperative to understand the impact of the introduction of O. sewalli on native populations of intertidal fish, such as the goby Bathygobius soporator. The impact of the non-native cryptobenthic species on the detritus food web may directly affect biodiversity and benthic habitats and lead to fundamental disruptions of the aquatic ecosystem and economic activities such as oyster aquaculture (Vieira et al., Reference Vieira, Baptista Neto, Crapez, Gaylarde, Pierri, Serrano, Bainy, Nogueira and Fonseca2021). Our results indicate a good application of FARMS as a monitoring tool for the rapid detection of invasive cryptobenthic fish, since we retrieved the O. sewali after one month. So the FARMs showed a valuable tool for future use in integrative taxonomical studies to answer whether there was only one introduction event of O. sewalli or multiple introductions on the Southeast-South Brazilian coast.
Acknowledgements
The authors are grateful for funding from the project National Council for Scientific and Technological Development and Fundação Araucária, Center for Marine Studies by the infrastructure and boats. The authors would like to acknowledge the schools Escola Municipal do Campo de Amparo and Colégio Estadual do Campo da Vila de São Miguel for their partnership with the citizen science and cryptobenthic fish project. B.M.C. acknowledges the National Council for Scientific and Technological Development (CNPQ 168196/2022-0). L.M.G. is thankful to Fundação Araucária. M.D.D. acknowledges the National Council for Scientific and Technological Development (CNPQ 312212/2020-8).
Author Contributions
Barbara Maichak de Carvalho – article design, sampling, analysis, writing and revision;
Luana Moroski Grein – sampling and writing;
Aron Davi – sampling and writing;
Maikon Di Domenico – writing and revision.
Financial Support
National Council for Scientific and Technological Development.
Competing interest
The authors declare no conflict of interest.
Data Availability Statement
Data are available on request from the authors.
