First report of the non-native gulf toadfish Opsanus beta (Goode & Bean, 1880) on the coast of Rio de Janeiro – Brazil

Biological invasions are considered an extreme risk to biodiversity, resulting in serious ecological and economic problems. Marine species have been introduced mainly through ballast water in estuaries, bays and inland waters, those bodies are historically threatened by intense urbanization making them highly susceptible to invasions. The gulf toadfish, Opsanus beta has been reported as an invasive species that commonly inhabits shallow water bodies, such as coastal bays and estuaries. Its native distribution range from Belize to Palm Beach – Florida (Gulf of Mexico). The first occurrence of O. beta on the Brazilian coast was in Santos estuarine area, Southeastern region, and the second was further south, in the estuarine complex of Paranaguá, Southern region. Here we report the first occurrence of a single O. beta in Rio de Janeiro coast, which was caught in October 2017, using a beach seine in Bica Beach, a polluted sandy beach located in Guanabara Bay – RJ. Considering the similarities among Guanabara Bay and other areas in Brazil, there is a potential for the establishment of O. beta populations in Guanabara Bay in a near future.


Introduction
Since the facility of traveling across geographical barriers has been growing with the globalization in the past 200 years, one of the most serious ecological and economic problems has been the introduction of non-native species (Perrings et al. 2005;Seebens et al. 2017). Biological invasions, characterized by the establishment of introduced species and their subsequent impacts over the ecosystem, are considered an extreme risk to biodiversity (Vitousek et al. 1997;Sala et al. 2000). In the marine realm, species have been introduced mainly by ballast water worldwide along the take up and release of these waters in estuaries, bays and inland waters, spreading non-native species to these environments. A great part of these water bodies are historically threatened by intense urbanization (e.g. the Guanabara Bay in Rio de Janeiro) and, consequently, water degradation, making them highly susceptible to invasions (Carlton and Geller 1993;Ruiz et al. 1997;Williams and Grosholz 2008).
The gulf toadfish Opsanus beta (Goode & Bean, 1880) (Batrachoididae) has been reported as an invasive species that commonly inhabits seagrass beds and rocky shores in shallow water bodies, such as coastal bays and estuaries (Robins and Ray 1986). Its native distribution ranges from Belize to Palm Beach -Florida (Gulf of Mexico) (Collette 2002). Here we report the first occurrence of O. beta on Rio de Janeiro coast, Southeastern Brazil. This paper is part of a long-term and broad study that aims to address the spatial changes of fish assemblages along the estuarine gradient of Guanabara Bay.

Materials and methods
Guanabara Bay, the second largest bay in Brazil, is a highly impacted estuarine system located on the coast of the State of Rio de Janeiro, one of the most populated urban areas of the world, home to circa 11 million people. Covering a surface area of 381 km² and 22 islands (Fistarol et al. 2015), Guanabara Bay harbors one of the most important ports in Brazil, handling over 5 million tons cargo in 2017 (ANTAQ 2017).
This study was conducted in nine beaches along Guanabara bay and was sampled bimonthly from October 2017 to July 2019. A single gulf toadfish was caught at Bica Beach (22°49′31″S; 43°10′06″W - Figure 1), a polluted sandy beach (~ 1 km long) located in the south of Governador Island, one of the most degraded areas in Guanabara Bay, located within a region of poor water quality (Fistarol et al. 2015). Fish were surveyed using a beach seine with a bag (20 m width × 2 m height; 7 mm mesh size). The beach seine was set parallel to the coast and hauled perpendicularly to the shore by a distance of 20 m (up to 3 m depth), resulting in an approximately 400 m 2 fishing area. Before the seine haul, water temperature, dissolved oxygen, salinity and pH were measured using a multi-parameter probe Hanna HI 9828 and transparency was assessed through a Secchi disk.
Opsanus beta was dissected in the Laboratory of Theoretical and Applied Ichthyology at the Ecology and Marine Resources Department of the Federal University of the State of Rio de Janeiro (UNIRIO). The fish was measured for total length (cm; TL) and total weight (g), of which gonads and stomach were weighed and preserved in 10% buffered formalin. The stage of gonad maturation was macroscopically classified following Núñez and Duponchelle (2009).

Results
The single sampled individual of Opsanus beta was captured in October 2017 and measured 19.4 cm (TL) and weighed 136.31g ( Figure 2). In order  to confirm the taxonomy, the morphometric characteristics of the fish were taken and compared with the results of other studies in both native and non-native ecosystems ( Table 1).
The gonads of the captured individual weighed 5.69 g and were of a recently spawned female since they were still relatively large and flaccid with remaining spaces and oocytes (Figure 3). This stage is characterized by the presence of developing yellow (vitellogenic) oocytes of different sizes and intense vascularization at the distal part, which may indicate the beginning of new spawning cycles until the end of the breeding season.  (Collette 2001). Standard length (mm) and counts of fish body parameters in raw data, other body measurements as given proportions in thousandths of standard length (‰ SL) (Adapted from Caires et al. 2007  Two genera of brachyuran Acantholobulus sp. and Achelous sp. (Figure 4) were observed within stomach contents, weighing in total 1.901 g, beyond 1.273 g of non-identified organic material. In addition, there was plastic and hair fragments inside the stomach (Figure 4).
The abiotic conditions at Bica Beach measured at the moment wherein the specimen was captured were: water temperature 24.37 °C, dissolved oxygen 1.6 mg/L, salinity 32.98 PSU, pH 8.30 and transparency 80 cm.

Discussion
Identifying which species has the highest potential to establish itself and the most susceptible sites for invasion are fundamental questions for the study of bioinvasions (Mack et al. 2000). Such information could provide more effective prevention actions, while on the other hand, once established, it takes larger efforts and costs to control and mitigate its impacts (Kolar and Lodge 2001). The probability that a species survives and spreads depends on the interaction of a series of factors, involving the environmental conditions and biotic resistance (e.g. community diversity, tolerance thresholds, predators and competitor abundances) (DeRivera et al. 2005). In addition, if the non-native species is a dissimilar predator to native ones, it will likely not be recognized as menace by native prey and, as a prey, to native top predators (Sih et al. 2010).
The first occurrence of O. beta along the Brazilian coast (see ) occurred in Santos estuarine area (23°58′56″S; 46°17′22″W). Although  erroneously described it as a new species named O. brasiliensis, Caires et al. (2007) concluded that it was a junior synonym of O. beta and registered the first occurrence further south, in the estuarine complex of Paranaguá (25°29′07″S; 48°26′15″W), in the State of Paraná (Figure 1). It is also suggested that, since the records of this species are close to port areas, ballast water might be responsible for its introduction. Tomás et al. 2012 concluded that O. beta is probably already established in Santos estuary and can be considered a severe threat to native diversity not only at this place but to any other estuarine system.
Opsanus beta is an ambush predator of many groups including fishes and invertebrates, in both native and non-native environments (Tomás et al. 2012;López et al. 2017). The crab genus Achelous found in the stomach contents in this study is considered commercially valuable in Guanabara Bay (Moreira et al. 2011), a fact that can amplify the future impacts of this hypothetical invasion. Furthermore, two species of fishes (Citharichthys spilopterus Günter, 1862 and Gobionellus oceanicus Pallas, 1770) that were found in stomach contents of O. beta at its native area (López et al. 2017), can also be found in Guanabara bay (Silva et al. 2016). The occurrence of plastic and hair fragments in the stomach emphasizes the voracious nature of this predator, probably ingested while preying on the crabs.
Reproduction of O. beta starts when male specimens nest and attempt to attract females with courtship vocalization, and after fertilization males guard the nest (Barimo et al. 2007;López et al. 2017). The type of spawning ranges from batch (Florida, USA (Barimo et al. 2007) and Paraná, Brazil (Nagata 2013)) to single spawning in Florida (Malca et al. 2009). Another difference found in literature was the period of spawning. Barimo et al. (2007) detected winter and spring as spawning seasons and López et al. (2017) observed spawning during summer (Veracruz, México) in its native area (Florida, USA), while Nagata (2013) described O. beta as an all-year-long spawning species. Those differences might be attributed to different seasonal abiotic variations among the studied areas and show O. beta ability to adapt to different environments.
According to Breder (1941), the length at first maturity of this species is 9.5 cm, which indicates that the captured individual is an adult able to reproduce, also evidenced by the developed gonads. Since the macroscopic stage of maturity of the gonads was classified as spawned, it is possible to infer that the species has been spawning in Guanabara Bay.
Several studies showed that O. beta is adapted to a wide range of conditions regarding water temperature (18.9 to 32 °C), salinity (8 to 39 PSU) and dissolved oxygen (4.1 to 11.4 mg/L), occurring in costal water bodies, such as bays and estuaries, with spatial and seasonal variations (Serafy et al. 1997;Barimo et al. 2007;López et al. 2017). Male toadfish can take advantage of pollution by using human waste (cans, plastic containers) as shelter when guarding the nest (Ryder 1886;Gill 1907).
Finally, considering the similarities among Guanabara Bay and other areas in Brazil where the species is considered established (see Tomás et al. 2012), the potential establishment of O. beta in Guanabara Bay raises concern. Therefore, actions to avoid the arrival and spread of other individuals, leading to further population establishment and massive invasion in this highly disturbed system are extremely important. However, to be sure of the establishment and its potential impacts, which are key factors to assign this species as invasive, further studies focusing on the ecology of this species are needed, thus requiring larger numbers of individuals, not recorded through our surveys. It is important to mention that our sampling method (beach seine) is not the most appropriate, neither our aim, to catch O. beta, since, beaches are not the common habitat of this species (Robins and Ray 1986).