Predation on the invasive swimming crab Charybdis hellerii (Crustacea, Decapoda) by Myrichthys ocellatus (Actinopterygii, Ophichthidae): the first record of consumption by a native fish

ABSTRACT Charybdis hellerii is an invasive swimming crab widely disseminated in the western Atlantic. This species became a threat to colonized ecosystems, competing with local species for resources. The extension of distribution and increasing population size of C. hellerii has been associated with the scarcity of indigenous predators and cases of predation report octopuses as the main native predators. In this study, we present the first evidence that native fish can consume C. hellerii. 53 individuals of the goldspotted snake eel, Myrichthys ocellatus, were collected at seagrass and macroalgal beds in Pernambuco State, Brazil, and had their stomach contents analyzed. Three juvenile C. hellerii were found along with native prey. Myrichthys ocellatus feeds mainly on small crabs, thus C. hellerii individuals were consumed before reaching sexual maturity. Oppositely to octopuses and other crab predators, M. ocellatus is of little fishing interest and is commonly found in macroalgae beds, seagrass meadows and sandy areas near reefs. Our results suggest that a higher number of carcinophagous taxa may prey on this invasive crab and we emphasize that the conservation of these species is paramount for controlling C. hellerii populations in invaded areas.

Charybdis hellerii has colonized the Atlantic Ocean through the Mediterranean Sea with the opening of the Suez Canal, reaching the western Atlantic by the end of the 80`s [13]. This species spread along the Caribbean in the following years, probably transported by ballast water and local currents [14,15]. The rapid growth, continuous reproduction, along with the generalized habitat and diet requirements of C. hellerii, allowed a successful establishment and spread of this IAS, which is now found in virtually the entire Brazilian coast, from Pará to Santa Catarina states [13,16].
Local impacts caused by C. hellerii are still underreported; however, available literature indicates potential economic and biological effects [10]. In Twin Cays, Belize, this crab is possibly displacing other decapods previously found in higher abundances at the area (e.g. spider crabs (Mithrax spp.), swimming crabs (Callinectes spp.) and spiny lobsters (Panulirus spp.)) [17]. In some Brazilian states (e.g. São Paulo and Santa Catarina), C. hellerii has outnumbered local crab populations, competing for resources with native species [4,16]. The use of this invasive crab in local fisheries is minimal; for example, in Venezuela (Falcón State), C. hellerii represented 5% of the captures in crab artisanal fisheries in 2003-2004 [18]. Moreover, C. hellerii was also identified as a potential host for the white spot disease virus, which causes high mortality in shrimp [10].
In spite of the complexity of processes that underlie biological invasions, IAS success can be linked to reduced population control by predators (i.e. the enemy release hypothesis) [19][20][21]. In fact, the instances of predation on C. hellerii by indigenous species are very limited and highlight octopuses as the most common consumers [22,23]. Here, we present the first report indicating that fish may act as predators of this invasive species. Predation on C. hellerii by CONTACT Maria Laís Martins Vieira laismvieira07@gmail.com native fish was revealed by the analysis of stomach contents of the goldspotted snake eel, Myrichthys ocellatus (Lesueur, 1825). This species is found from Bermuda and South Florida, in the Caribbean, to Santa Catarina, in Brazil [24,25]. Samples were collected on the beaches of Catuama (7°37ʹ40.7 "S; 34°48ʹ19.9" W) and Tamandaré (08º45ʹ35ʹ'S; 35º06ʹ17ʹ'W), located on the Northern and Southern coasts, respectively, of the State of Pernambuco, Brazil (Figure 1). The Catuama beach is influenced by the Itamaracá estuarine complex and comprises the largest seagrass meadows in the region where individuals of M. ocellatus were captured. Tamandaré, on the other hand, is part of the most extensive marine protected area in the Brazilian coast, the Costa dos Corais Marine Protected Area. The Tamandaré reef complex includes one of the largest fringing reef formations in the South Atlantic. In this site, M. ocellatus was captured at the macroalgal beds adjacent to shallow reefs (also see study location in [26]). The goldspotted eel is very common in the study area [27,28], but there are no records of C. hellerii presence on both sites sampled prior to this study.
Individuals were captured during free dives performed between August and December 2019, on low tides at a maximum depth of 2 m, using hand nets (~40 cm diameter, 1.5 cm mesh). A total of 53 individuals were collected, 25 being captured in Catuama and 28 in Tamandaré, with sizes ranging from 33.5 to 66 cm in total length, with an average of 46.6 cm. After collection, specimens were fixed in a 4% formaldehyde solution. In the laboratory, stomach contents were removed on a petri dish and identified under stereo-microscope (40x magnification). Each individual prey was measured with a digital caliper (0.1 mm accuracy) and preserved in 70% ethyl alcohol.
Three individuals of Charybdis hellerii were found in the stomach contents of Myrichthys ocellatus (Figure 2). Specimens found were sexually immature; two males and a female measuring 11, 12 and 19 mm in carapace width (CW), respectively. The female was consumed by an individual of M. ocellatus with 47 cm of total length (TL) and one of the males was found as a prey of a fish with 39 cm TL, both collected in Catuama beach. The male with 11 mm CW was found within stomach contents of a 52 cm TL goldspotted eel sampled in Tamandaré.
Myrichthys ocellatus preys mainly on mobile invertebrates, especially crabs of the families Portunidae, Xanthidae and Majidae [27][28][29]. During our stomach contents analysis, we found that the bulk of M. ocellatus diet is composed by these native crab species (e.g., Callinectes spp., Pitho sp., Epialtus sp.), also registering the ingestion of mollusks, isopods and shrimps to a lesser extent. This is the first record of a native fish using C. hellerii as prey, suggesting that a higher number of carcinophagous taxa may feed on this invasive crab as well.
Oppositely to the predation performed by octopuses or larger fish, which target larger prey [23], M. ocellatus predates preferentially on small crabs, well below the size of first maturity for C. hellerii, which is approximately 37 mm CW for females [29][30][31][32]. Bearing in mind that each female of C. hellerii can produce from 22,500 to 3,200,000 eggs per reproductive event [14,33], the predation of this exotic crab before breeding can represent an effective way of local control of its spread [23].
Additionally, groupers, crabs and octopuses are of high fishing interest and their populations are in decline [34][35][36][37][38][39], while snake eels are of little economic value and are not fished at all [40]. One of our study sites, Catuama beach, is heavily targeted by fishing and show highly depleted fish communities when compared to other seagrass meadows in the region [41]. Yet, M. ocellatus seems to have high abundance in the area, and may contribute in preventing the local establishment of C. hellerii. Indeed, seagrass-associated macrofauna surveys in this study site does not show indications of established populations; in a previous survey performed in 2017 by our study group, 4,500 invertebrates were sampled and not a single individual of C. hellerii was captured [42].
The goldspotted eel is a crab predator found in various habitats, such as seagrass meadows, macroalgal beds, rocky shores and coral reefs [26][27][28]. It is also a conspicuous member of the ichthyofauna along a large extent of the area colonized by C. hellerii in the western Atlantic [43]. We hypothesize that M. ocellatus, along with other carcinophagous fish, may play an important role in the dynamics of C. hellerii invasion, to be evaluated in further studies. Our results emphasize the importance of the conservation of local carcinophagous species, given their potential role in the control of populations of this invasive crab.

Disclosure statement
No potential conflict of interest was reported by the author(s).