First report of predation by a small shark on the invasive rapa whelk Rapana venosa (Valenciennes, 1846) in Argentinean waters

The rapa whelk Rapana venosa (Valenciennes, 1846) has few predators in areas outside of its native range. Here we report the first incidence of predation by a small shark Mustelus schmitti Springer, 1939 on the rapa whelk in coastal waters of Argentina. This finding could give information about possible trophic control over R. venosa as it potentially disperses into coastal waters of Atlantic South America.


Introduction
Mustelus schmitti Springer, 1939 is a small-bodied shark endemic to the southwestern Atlantic Ocean from Florianópolis (27ºS,Brazil) to Bahía Grande (52ºS, Argentina) (Van der Molen et al. 1998;Chiaramonte and Pettovello 2000;Cousseau and Perrotta 2004). Mustelus schmitti is one of the most abundant species of elasmobranches in the northern Argentine coastal ecosystem (Jaureguizar et al. 2004), and an important fishing resource. This small shark is a demersal-pelagic predator with a diet comprised mainly of large decapods (Brachyura and Anomura), polychaetes, and, of particular importance for this study, whelks (Gastropoda: Buccinidae) (Bergonzi 1997;. The rapa whelk Rapana venosa (Valenciennes, 1846) is a large predatory gastropod native to the Sea of Japan, east China Sea, and Taiwan. It was first recorded in South America in 1998 from the Río de la Plata (RdlP) near Montevideo (Figure 1), and then it spread throughout the central estuary (Scarabino et al. 1999;Pastorino et al. 2000). Afterwards, it was found in Samborombóm Bay (south coast of RdlP, Giberto et al. 2006), throughout the entire RdlP estuary (Scarabino et al. 1999;Rodriguez-Capítulo et al. 2002), and more recently in nearby marine coastal waters of both Uruguay (Lanfranconi et al. 2009) and Argentina (Giberto and Bruno 2014). Due to its high fertility and the fact that the temperatures of the estuarine system are within the tolerance range for breeding, rapa whelk continues to spread, and is extending its distribution to the coastal area of Argentina such that it is now common as a by-catch of several fisheries (Giberto and Bruno 2014).
The effects of the rapa whelk on the functioning of the RdlP ecosystem is not understood but preliminary work indicates it affects multiple ecosystem components both directly and indirectly (Lercari and Bergamino 2011). For example, the rapa whelk often preys upon economically important bivalves. Within the RdlP and adjacent marine waters, the spatial distribution of R. venosa matches with the distribution of commercially important native bivalves, i.e., Mactra isabelleana d'Orbigny, 1846 and Ostrea puelchana d'Orbigny, 1842, and it likely preys upon these species (Giberto et al. 2006). Such predation could have negative socio-economic consequences (Lercari and Bergamino 2011). In addition, R. venosa shows high diet overlap with the Whitemouth croaker Micropogonias furnieri (Desmarest, 1823), an important finfish coastal resource, and that raises the possibility of competition for food.
The rapa whelk has relatively few predators in invaded locations. The blue crab Callinectes sapidus Rathbun, 1896 is capable of preying upon small Rapa whelks, at least in the laboratory (Harding 2003). Under natural conditions in the RdlP estuary, adult loggerhead turtles Caretta caretta (Linnaeus, 1758) can consume large numbers of rapa whelks (Carranza et al. 2010) in addition to their normal diet of benthic invertebrates (crustaceans and mollusks) and fishes discarded from coastal fisheries (Estrades et al. 2007;Martinez-Souza 2009). In the RdlP estuarine waters, R. venosa has higher densities than in the outer marine coastal waters; however, its abundance is increasing (Giberto and Bruno 2014), which could make it an attractive prey to marine benthic feeders. However, until now, there was no evidence of predation on rapa whelks in the neighboring marine coastal waters of RdlP, and there are no reports of predation by fish in invaded habitats worldwide (Harding 2003;Carranza et al. 2010). This paper is the first report of predation by a shark on R. venosa in the outer marine coastal water of RdlP and discusses the results in the context of the ecological features of both species.

Methods
The small-scale fishery located in Punta Médanos (36º53′S, 56º39'W; Figure 1) is mainly conducted in fully marine waters, but there are low salinity extensions of the RdlP plume during summer months (Jaureguizar et al. 2015). This small-scale fishery uses small fiberglass boats and employs nylon gillnets (stretched mesh ranging from 90 to 120 mm and 2 m in height). During spring, the average (± SD) soak time is 17.8 ± 6.5 h, average length of net is 511.6 ± 251.4 m, and the average distance to the coast is 3.4 ± 2.05 km (Jaureguizar et al. 2015).
A small number (n = 28) of Mustelus schmitti were collected during October 2012. The shark specimens were between 565 and 774 mm total length (TL) and captured in waters < 10 m deep. Whole sharks were transported to the laboratory, stomachs were dissected, and then total stomachcontent weight was recorded. The prey items were identified to the lowest possible taxonomical level, counted, and weighed.

Results
All 28 stomachs analyzed contained food, 21 prey taxa in total. In terms of percent by number, the principal prey were polychaetes (Family Glyceridae) at 34%; hermit crabs Pagurus sp. at 18.3%, and unidentified polychaetes at 12.4%. When expressed as % wet weight, the main prey were unidentified crabs (50.2%), the squid Doryteuthis sanpaulensis (Brako-niecki, 1984) (18.4%), and hermit crabs (17.9%). One shark 651 mm TL contained a rapa whelk operculum (23 mm longest axis; Figure 2A) along with some of the body tissue. Based on a published regression equation (Carranza et al. 2010), this corresponded to a rapa whelk of 58 mm shell length.

Discussion
The shark M. schmitti feeds opportunistically upon benthic prey, typically crustaceans, polychaetes, and fishes . Gastropds are a secondary prey and, like other sharks, hard and soft parts are reported in stomach contents (Vögler et al. 2003). Considering the feeding strategy and dentition of M. schmitti , the finding of remains, including an operculum, of R. venosa did not seem to be an accident.
Rapana venosa occurs mostly in estuarine waters of RdlP, and its abundance abruptly decreases along the adjacent marine coastal waters as one moves away from the RdlP mouth (Giberto and Bruno 2014). The differences in predation upon R. venosa between loggerhead turtles and the small shark in the RdlP area reflects differences in distribution of the two predators. Loggerhead turtles occur more in the estuarine area while M. schmitti mainly inhabits the outer coastal waters in salinities 28-30 (Cortés 2012). These salinities represent the outer salinity front of RdlP (Lucas et al. 2005) and correspond to the boundary for marine species intrusions into the estuary (Jaureguizar et al. 2003(Jaureguizar et al. , 2004(Jaureguizar et al. , 2006. Given that only a few shark stomachs were collected, clearly there is need for additional sampling to assess the potential role of M. schmitti as a predator of rapa whelks. Moreover, we currently cannot rule out the possibility that the shark in this study scavenged a whelk discarded by a commercial fishery. The two hypotheses, of course, are not mutually exclusive. Other potential predators of this exotic mollusc include demersal fishes as Micropogonias furnieri, which also feeds on benthic prey, such as polychaetes, gastropods and bivalves (Puig 1986;Giberto 2001;Giberto et al. 2006;D'Anatro et al. 2013). The similarity in diet between the fish and whelk also raises the possibility of a competitive interaction should the whelk become abundant enough for food to be limiting. However, to date R. venosa had not been found in stomach contents of any other predator in the outer marine coastal water of RdlP. As the rapa whelk population continues increasing and spreading, it would be useful to assess whether potential predators begin consuming this invasive gastropod and to examine the changing role of this invasive whelk in the coastal ecosystems, including studies conducted during different seasons of the year.